Annals of the New York Academy of Sciences - Furness Et Al-2015

8/18/2019 Annals of the New York Academy of Sciences - Furness Et Al-2015

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Ann. N.Y. Acad. Sci. ISSN 0077-8923

A N N A LS O F T H E N E W Y O R K A C A D E MY O F S C I E NC E SIssue: The Year in Evolutionary Biology

Reproductive mode and the shifting arenas of evolutionary

conflict

Andrew I. Furness,1,2 Keenan R. Morrison,1 Teri J. Orr,1,3 Jeff D. Arendt,1

and David N. Reznick1

1Department of Biology, University of California, Riverside, California. 2 Department of Ecology and Evolutionary Biology,

University of California, Irvine, California. 3 Department of Biology, University of Massachusetts, Amherst, Massachusetts

Address for correspondence: Andrew I. Furness, Department of Ecology and Evolutionary Biology, 321 Steinhaus Hall,

University of California, Irvine, CA 92697. [email protected]

In sexually reproducing organisms, the genetic interests of individuals are not perfectly aligned. Conflicts among

family members are prevalent since interactions involve the transfer of limited resources between interdependentplayers. Intrafamilial conflict has traditionally been considered along three major axes: between the sexes, between

parents and offspring, and between siblings. In these interactions, conflict is expected over traits in which theresulting

phenotypic value is determined by multiple family members who have only partially overlapping fitness optima.

We focus on four major categories of animal reproductive mode (broadcast spawning, egg laying, live bearing, and

live bearing with matrotrophy) and identify the shared phenotypes or traits over which conflict is expected, and

then review the empirical literature for evidence of their occurrence. Major transitions among reproductive mode,

such as a shift from external to internal fertilization, an increase in egg-retention time, modifications of embryos

and mothers for nutrient transfer, the evolution of postnatal parental care, and increased interaction with the kin

network, mark key shifts that both change and expand the arenas in which conflict is played out.

Keywords: antagonistic coevolution; genomic imprinting; inclusive fitness; kinship theory; mating system; matrotro-phy; oviparity; parent–offspring conflict; placenta; sexual conflict; siblicide; viviparity

Introduction

The family dynamic is characterized by a webof interactions between interdependent players:mothers and fathers, parents and offspring, andamong siblings1–5 (Fig. 1). The traditional view isthat these family interactions involve cooperation

geared toward the maximization of offspringproduction. However, with the formalization of inclusive fitness theory,6,7 this view was eventually overturned. In its place came the realization thatsuch interactions involve both cooperation and

conflict, the scope of which is dictated by therelatedness of the players involved and hence thedegree to which their genetic interests coincide.6–9

Sexual reproduction creates the potential forconflict as alleles in males, females, and offspring

each have their own optimal phenotypic effects ontraits involved in the allocation and acquisition of

parental investment10,11 (Fig. 2). When will conflictbe realized and over what traits will family membershave different fitness optima? Our contention isthat reproductive mode and mating system togetherdetermine the extent and context in which parentsand offspring interact, thereby dictating over what

fitness-related phenotypes antagonistic selectioncan act. Specifically, reproductive mode (includinglocation of fertilization, where embryonic devel-opment occurs, and parental care) governs in whatphysical arenas, at what time points in an organism’slife history, and over what traits conflict may beexpected.1,12

This interaction between reproductive mode andthe potential for conflict is illustrated in the study of offspring size at birth in species with different

reproductive modes. Janzen and Warner13

measuredselection on egg size in three species of turtles and

doi: 10.1111/nyas.12835

1Ann. N.Y. Acad. Sci. xxxx (2015) 1–26 C 2015 New York Academy of Sciences.


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Reproductive mode and evolutionary conflict Furness et al.

Figure 1. Illustration of the interactions that define family conflict. Male–male competition occurs among males for access to

mating opportunities. Sexual conflict occurs between males and females over whether to mate, mating rate, fertilizations, and

parental care. Parent–offspring conflict (as depicted here) occurs between the mother and offspring over resource use, growth rate,

birth size, and cooperativeness with kin. Sibling conflict occurs between siblings over resource use and growth rate. Multiple mating

and the resulting mixed paternity litters (depicted as offspring of different colors) intensify family conflict. Figure modified after

Parker et al.4 and Kamel et al.1

were able to generate maternal and offspring fit-

ness surfaces on the basis of hatchling survival. Inthe softshell turtle (Apalone mutica ), the egg sizethat maximized individual offspring fitness was onestandard deviation greater than the egg size thatmaximized maternal fitness. In turtles, as in many organisms, there is a tradeoff between offspring sizeand offspring number14,15 in that a mother canproduce many small eggs or fewer larger eggs. Indi-vidual offspring have higher survival if they are abit bigger. However, a mother maximizes her netreproductive output by producing slightly smaller

eggs and thereby being able to produce more eggs,essentially accepting slightly higher mortality risk per individual offspring in order to maximize herown fitness. In the softshell turtle, the populationmean egg size was almost perfectly coincident withthe maternal optimum.13 The authors’ interpreta-tion of this result is rooted in parent–offspring con-flict theory (see also Ref. 16). Turtles provision theireggs before fertilization so that egg size is deter-mined solely by the maternal genome. Thus, alleles

expressed in offspring cannot influence their ownprovisioning (i.e., egg size). Therefore, although

the difference in optimal egg size between mother

and offspring yields an expectation of conflict,mothers have complete control over the outcome.13

Conversely, placental species begin with relatively small unfertilized eggs and offspring gain substan-tial weight over the course of development.17–19 Inthese species, theexpressionof theoffspringgenomeoverlaps with the timeframe during which offspringare provisioned, thus providing ample opportunity forallelesexpressedinoffspringtoinfluencelevelsof maternal investment. The role of offspring genotypein governing birth size has been demonstrated in

mammals20,21 and placental fish,22 where investiga-torshave performed reciprocal crosses between pop-ulations/species that differ in offspring size. Fromsuch reciprocal crosses, it is clear that offspringgenotype has a large effect on size at birth, ratherthan being solely a trait under maternal control. Inother words, offspring are not merely passive vesselsin which parental resources are poured but actively manipulate their own provisioning. Thus, for pla-cental organisms, size at birth represents a shared

trait potentially subject to parent–offspring conflict(Fig. 3).

2 Ann. N.Y. Acad. Sci. xxxx (2015) 1–26 C 2015 New York Academy of Sciences.


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Furness et al. Reproductive mode and evolutionary conflict

Figure 2. Optimal offspring size at birth in mice from the perspective of four interacting alleles that can potentially influencethis trait (from left to right): mother (or maternal alleles), a maternal allele in the offspring, the offspring (alleles in offspring

irrespective of parent of origin), and a paternal allele in the offspring. Parent–offspring conflict is expected when the phenotypic

value lies between the maternal and offspring optimum. Parent-of-origin specific gene expression may evolve when the phenotypic

value is between the optimum for maternal and paternal alleles in offspring. Figure modified after de Jong and Scott.10

From the inception of the concept of interge-nomic conflict, it has been apparent that repro-ductive mode determines the context and degreeto which family members interact and thereby gov-erns the opportunity for evolutionary conflict (and

cooperation). The exponential growth of empiricaland theoretical studies has fleshed out the scope anddiversity of such conflicts. Conflict is theoretically possible in multiple physical arenas, over a variety of sharedtraits,andcanresultinamultitudeofadapta-tions and counteradaptations through antagonisticselection. Yet, such conflict is not equally likely tooccur in different taxonomic groups that have dif-ferent mating systems and modes of reproduction.Consideration of reproductive mode allows for the

generation of targeted predictions regarding the tis-sues, life history stages, and traits over which con-flict is expected (Tables 1 and 2). We first providebrief background on different categories of conflict(sexual, parent–offspring, and sibling) and theirinteraction, and then provide an introduction toreproductive mode. Finally, we highlightsome of themore theoretically and empirically well-exploredmanifestations of conflict within four major cat-egories of animal reproductive mode (broadcastspawning, egg laying, live bearing, and live bearing

with matrotrophy).

Different forms of family conflict

Sexual conflict Sexual conflict occurs when males and females haveincompatible fitness optima related to courtship,mating, fertilization, offspring provisioning, andparental care.23–26 Conflicts between the sexes arerooted in differing reproductive roles and inequal-ities in net investment in offspring.23,27 Specifi-cally, the sex that invests less in reproduction andparental care (typically males) has more to gainfrom mating and fertilization because the oppos-ing sex will be in limited supply.28–32 Furthermore,unequal investment in reproductive processes oftencauses the sexes to differ in the costs of mating andreproduction.33–35 These differing costs and bene-

fits can lead to sexually antagonistic selection if theevolution of the optimum in one sex is gained atsome cost to the opposite sex.23,24,26,36,37 Antagonis-tic selection has led to the evolution of an array of behavioral, morphological, and physiological adap-tations (and counteradaptations)for control of mat-ing and fertilization.23,24,38 This conflict persistsin species that exhibit postfertilization biparentalinvestment in offspring because each sex benefitsfrom the other providing additional investmentwhile at the same time limiting its own investmentin favor of future opportunities to reproduce.39–41



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Figure 3. Graphical and metaphoricaldepiction of parent–offspring conflict. Mother and offspring exhibit different fitness optima

for the phenotypic value of the shared trait (i.e., birth weight or any other trait that involves parental investment). When both

parties are evenly matched or compatible, analogous to a tie, the phenotype ends up within a range of variation that we consider

normal. However, perturbation of this unsteady equilibrium can result in a mismatch or incompatibility, which is analogous to one

side winning the tug of war and dragging the shared phenotype outside the range of normal variation, something that could be

maladaptive for both parties (ideas based on Wilkins65 and Frank and Crespi64).

Parent–offspring conflict Offspring share only half of their genes with theirmother, whereas mothers are equally related to eachof their offspring. Thus, individual offspring benefitdisproportionately (and maximize their own inclu-sive fitness) by acquiring a larger share of maternalresources than she is generally willing to devote toany single offspring.9 In short, mothers seek to max-imize the total number of offspring produced over alifetime,42 whereas each offspring seeks to maximizeits individual fitness. This puts motherand offspring

in conflict over the divvying up of resources and canlead to a tug of war in which each party uses what-ever means are available (physiological, hormonal,or behavioral) to reach its optimum.9,43 For exam-ple, during different periods of offspring ontogeny (prenatal versus postnatal), theeffectof gene expres-sion on investment may take very different forms.

In prenatal mammals, offspring are expected toemploy mainly physiological and hormonal means,likely at the placental interface,43,44 but after birth

a variety of behavioral responses, such as suck-ling and begging behavior, may elicit maternalinvestment.2,9,45

Sibling conflict Sibling conflict refers to competition or overtconflict between offspring over limited parentalinvestment.2 The underlying logic is similar to that

for parent–offspring conflict. Offspring share half of their genes with full siblings and one quarter of their genes with half siblings yet are fully relatedto themselves. A consequence is that individual off-spring maximize inclusive fitness by obtaining morethan merely sufficient parental investment, or beingselfish up until the point where the benefits derivedfrom continued parental investment are balancedby the costs imposed on their siblings.9 Siblicide,the most extreme form of competition between sib-

lings, is often present in nestling birds2,3

but can befound in a wide range of taxa and can even manifestas intrauterine cannibalism.46,47 Sibling conflict is



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Table 1. Shared traits over which conflict might be expected as a function of reproductive modea

Gestation

length (as Sociality Shared traits over which conflict might occur/adaptations

Physical proportion of In utero Post- (interaction reflecting a history of antagonistic selection

Reproductive l ocation of embryonic maternal hatching with kin Example Parent–offspring

mode fertilization development) provisioning parental care network) taxa Sexual conflict conflict Sibling conflict

Ovuliparity External N/A N/A No Little to none Broadcasting spawning

marine fishes and

invertebrates

Gamete traits, sperm–egg

interaction, rate of

fertilization

None None

External N/A N/A Yes Some Poison dart frogs,

mouthbrooding cichlids,

nest-guarding fish

Gamete traits, sperm–egg

interaction, rate of

fertilization, mating

interactions

Filial cannibalism (parents

eating offspring)

Space use, aggregation

behavior,

altruistic/competitive

interactions between

siblings, sibling

cannibalism

Oviparity Internal Partial None No Little to none Many insects, including

Drosophila , most lizards

and snakes, turtles

Physical control of mating,

mating frequency and

duration, sperm

storage/removal,

copulatory plug

formation, seminal

proteins’ effect on female

behavior and physiology,

sperm–egg interactions,

rate of fertilization

Duration of brood

retention

None

Internal Partial None Yes Yes Birds, monotremes " Offspring growth

rate/begging behavior,

fledging date, dispersal

behavior

Space use, aggressiveness

toward siblings and

resource competition,

siblicide

Lecithotrophic

viviparity

Inter nal Complete Limited

(passive

diffusion)

No Little to none Some fish, sharks and rays,

snakes, lizards, and

amphibians

" Timing of birth None

Matrotrophic

viviparity

Internal Complete Extensive No L ittle to none Placental fish, lizards,

sharks, and invertebrates

" Embryo abortion,

implantation, in utero

nutritional supply and

growth rate, gestation

length and birth size

Competition over maternal

investment during

gestation, intrauterine

cannibalism

Internal Complete Extensive Yes Yes Mammals " ", Infanticide, postnatal

growth rate, suckling

behavior, solicitation of

nursing, size and date of

weaning, dispersal

behavior, cooperative

breeding, resource

sharing

", Competition for maternal

milk, kin recognition,

cooperative and

aggressive behavior

toward siblings (i.e.,

huddling, siblicide)

a We define a shared trait as the phenotype or trait over which conflict occurs, when the resulting outcome is the product of the

interaction between players who have only partially overlapping genetic interests.24,317

predicted to be most intense with multiple pater-nity, which reduces the average genetic relatednessamong siblings from one half to one fourth. It is alsointensified in species with postnatal care if resourcesare limiting, offspring differ in their competitiveabilities, there is hatching asynchrony, or parentalfavoritism.2,48–50

Relationships among forms of conflict, factors

limiting or exacerbating conflict, and conflict resolution Taking a “gene’s eye view” blurs the lines betweenotherwise seeminglydiscreetcategoriesof conflict—all forms of family conflict may occur simultane-ously with their resolution reflecting the sharedand competing interests of all parties.1,2,4 In inter-actions between mother and offspring, four typesof genes are potentially involved, each with theirown optimal phenotypic effects on the shared trait:genes expressed in the mother, maternally inher-ited genes expressed in offspring, paternally inher-ited genes expressed in offspring, and offspring

genes expressed regardless of the parent of origin(Fig. 2). An active area of theoretical research is theprediction of optimal rates of investment for thedifferent participants in this complex network of interfamilial relationships.4,10,51 One theme thatpervades the conflict literature is the potentialfor escalation resulting in an arms race whereadaptation on one side is countered by adap-tation in the other.12,37,52–54 Like other dynamic

systems that involve multiple coevolving players,predicting the resolution of conflict can be difficultbecause it is sensitive to starting assumptions, mech-anisms available to each party, and the balancingof costs and benefits between multiple interactingplayers.24,26,38,55 Theory clearly defines factors thatcan exacerbate family conflict: promiscuous matingsystems where multiple paternity is common, largedisparity between the sexes in parental investment,ability of offspring to influence or solicit parental

investment, possibility of within-brood competi-tion, differences in offspring quality or competi-tiveness, small clutch size, and low relatedness of



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Table 2. Hierarchical organization for the expression of family conflicts

Physical arena of sexual, parent– Shared traits overoffspring, and/or which conflict might Adaptations affecting Predicted manifestationssibling conflict Level of selection be expected shared trait of conflict References

Mat ing are na Ma te ch oice Wh et he r to mate Male courtship, sensory bias,dishonest signaling,alternative reproductive

strategies, coercive mating,sneak copulations; femalepreference and matediscrimination

Female resistance to (at leastsome) male mating attempts,evolution of postcopulatory

sexual selection if fertilizationis internal

Arnqvist and Rowe,23

Chapman,24 King et al.,39

Neff and Svensson101

Mating (frequency and duration)

Male morphologicaladaptations for physically controlling mating,including graspingstructures, copulatory organs that contain hooksor spines, copulatory plugs,and mate guarding; femaledefensive structures,labyrinthine reproductivetracts, and insensitivity tomale effects

Mating above a threshold levelwill entail significant femalecosts and female adaptationswill mitigate or minimize suchcosts; correlated evolution of male and female morphology

Arnqvist and Rowe,23,52,53

Stockley,156 Chapmanet al.,319 Chapman,24

Brennan et al.110

Female reproductivetract

Sperm competitionand cryptic female

choice

Sperm storage,removal, and usage

Male seminal proteins thataffect female physiology

and behavior; spermviability, motility, andcompatibility with femalereproductive tract; femalephysical removal,sequestration, storage,destruction or selective useof sperm

Male seminal proteins willmanipulate female behavior

and physiology for the benefitof the male (and his offspring),for example, by increasingcurrent egg production andinhibiting additional mating.Such effects will entail femalecosts, such as reduced survival.Frequency-dependent selectionand/or rapid evolution in maleand female reproductiveproteins and high levels of interspecific divergence; femaletraits and organs that enhancesperm storage and choice

Arnqvist and Rowe,23

Parker,77 Stockley,156

Panhuis et al.,92 Orr andZuk 122,154

Fertilization Genetic and physiologicalsperm–egg interactions(genomic compatibility and immune recognition

loci), sperm viability, andmotility

Rapid evolution of reproductiveproteins and/orfrequency-dependent genotypeselection; sperm adaptations

that favor speed of penetrationand female egg adaptations thatslow this process, thus limitinglethal polyspermy

Frank,87 Panhuis et al.,92

Ramm et al.,155 Kamelet al.86

Early embryoabortion

Interaction between maternaland paternal genotype(genomic compatibility atimmune recognition loci),overproduction of hormones

Embryo abortion will be high;aborted embryos will bedefective or mismatched withmaternal immune loci (orother evidence of embryoselection, such as biased sex ratio or paternity bias);embryos may express highlevels of certain hormonesfrom an early stage to advertiseviability.

Diamond,164 Haig,43

Wedekind,120 Zeh andZeh,150–152 Stockley 157

Placenta/womb Selective implantationand differential

allocation toembryos

Implantation Interaction between maternaland paternal genotype

(genomic compatibility atimmune recognition loci),overproduction of hormones

Embryo abortion will be high;aborted embryos will be

defective or mismatched withmaternal immune loci (orother evidence of embryoselection); embryos may express high levels of certainhormones from an early stageto advertise viability.

Haig,43 Kozlowski andStearns,158 Zeh and

Zeh,150–152 Møller159

Prenatal nutritionalsupply and growthrate

Placental architecture,trophoblast invasion of uterine lining, fetalhormone production tomanipulate maternalphysiology

Rapid interspecific phenotypicand genomic divergenceassociated with placentation;evidence of antagonism at thefetal–maternal interface;wasteful or otherwise puzzlingaspects of anatomy andhormone production that may be detrimental to maternalhealth (i.e., preeclampsia,hypertension); positive

correlation between degree of multiple mating (as indexed by testis mass) and fetal growthrate

Crespi and Semeniuk,12

Haig,43 Pijnenborget al.,245 Long,252

Garratt251

Continued



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Table 2. Continued

Physical arena of sexual, parent– Shared traits overoffspring, and/or which conflict might Adaptations affecting Predicted manifestationssibling conflict Level of selection be expected shared trait of conflict References

Gestation length andbirth size

Fetal hormone production,physiological interactionbetween mother and

offspring determinestiming of birth

High variance in birth weight;preterm birth commonplaceand more likely for male

offspring; mean birth weight inpopulation does not equalbirthweight at which offspringsurvival is maximized.

Jones,192 Haig,193 Vatten andSkjaerven,248 Clifton249

Nest/den Allocation of postnatal parentalcare

Postnatal nutritionalsupply and growthrate

Begging behavior, dishonestsignaling of need;competition amongsiblings for suckling, spaceuse, huddling behavior

Loud calling/begging, overtphysical competition for accessto suckling space, siblicide;competition and fetal growthrate predicted to be higher inpromiscuous mating systemsthat promote mixed paternity litters.

Trivers,9 Mock and Parker,2

Briskie et al.,281 Royleet al.,283 Hudson andTrillmich49

Weaning date and sizeat weaning

Offspring begging, crying,temper tantrums; maternalresolve and physicalstrength

Offspring will resist weaning;conflict will be minimal early during investment period asboth parent and offspringinterests are aligned and willbecome progressively more

intense closer to weaning asinterests diverge.

Trivers,9 Bateson,284 Foutset al.,286 Drake et al.285

Infanticide/siblicide Cooperative and aggressivebehavior

Siblicide more likely in mixedpaternity litters;infanticide/filial cannibalismwill increase parental fitnessand is more likely underresource limitation or if parentscan selectively cannibalizelower-quality offspring.

O’Connor,276 Mock andParker,2 Ebensperger,176

Klug and Bonsall58

Brain/social arena Cooperativeness andselective favoritismtoward kin

Dispersal fromparental territory

Offspring behavioralpropensity to stay inparental territory, dispersaldistance; parental behaviorthat encourages dispersal

Sex-biased dispersal dependentupon mating system and kingroups; parents favor dispersaland/or longer dispersaldistances than offspring.

Motro,289 Liberg and vonSchantz,293 Isles et al.,298

Starrfelt and Kokko290

Kin recognition,resource sharing,

communal nursing,cooperativebreeding, language

Parent-of-origin specific geneexpression (i.e.,

imprinting) in these andother traits that havedifferential effects onparental fitness

Paternally inherited loci promoteselfishness and

maternally-inherited locipromote cooperativeness withkin through either silencing oroverexpression (dependingupon the phenotypic effects of particular allele).

Li et al.,225 Isles et al.,298

Haig,222,229 Plagge

et al.,318 Crespi andBadcock,211 Crespi,223

Elliot and Crespi,206

Keverne and Curley,226

Wilkinson et al.,210 Úbedaand Gardner,230,231

Brandvain et al.,227 Pattenet al.219

mating partners.25,38,56–61 In particular, a highdegree of multiple mating (high promiscuity)increases family conflict by decreasing the level of genetic relatedness among offspring, thus promot-

ing more divergent interests in the acquisition of parental investment (i.e., more selfish behavior).In contrast, monogamous mating systems tend toalign the interests of both sexes while limiting orconstraining the expression of parent–offspring andsibling conflict by increasing genetic relatedness.As Crespi and Semeniuk 12 note: “parent–offspringconflict is constrained by the genetic relatedness and

mutual dependency of the interactants such thatit often involves a tug-of-war over resource allo-cation, with signs of conflict remaining more or

less covert unless the interactions between partiesare perturbed in some way.”43,44,62,63 The potentialfor such perturbation means that a mismatch in

competitive abilities between interacting players canlead to developmental pathology and high levels of phenotypic variance64,65 (Fig. 3).

Reproductive mode

One of the most immediately recognizable featuresof different taxonomic groups of organisms is theway in which they reproduce. Do they have exter-nal or internal fertilization? Do they lay eggs or givelive birth? Do they exhibit parental care? Variation

in these traits is present across multiple taxonomiclevels,17,19,66–72 and an array of specialized termi-nology has been developed to accurately encapsu-

late the remarkable diversity of reproductive modespresent across the tree of life.17,73 Our classifica-tion of reproductive mode includes the mode of



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Figure 4. The evolution of vertebrate reproductive mode. Ovuliparity represents the ancestral reproductive mode and is char-

acterized by eggs and sperm being shed externally. Oviparity is characterized by internal fertilization with eggs being laid, and

embryo development completed externally. Lecithotrophic viviparity is livebearing with no postfertilization maternal provisioning

of embryos. Matrotrophic viviparity is live bearing with postfertilization maternal provisioning of embryos, for example, by means

of a placenta.

fertilization, where embryonic development occurs,and the means by which offspring are nourished.73

With few exceptions, the animal kingdom is char-acterized by sexual reproduction,74 which likely is a requirement for the rise of family interac-tions and the potential for conflict.75 Within theanimal kingdom, the ancestral form of reproduc-

tion is apparently that of eggs and sperm shedexternally 73 (although see Long et al.76 for thesurprising suggestion that, in jawed vertebrates,broadcast spawning may be derived from inter-nal fertilization). The evolution of internal fertil-ization represents a necessary step on the path tomore derived reproductive modes.66 Parker77 pro-posed that internal fertilization likely evolved asa form of paternity assurance; males that couldlocate their sperm within the female would exhibit

a reduced chance of sperm competition and muchgreater chance of attaining paternity than if spermwere shed externally. Once eggs are fertilized inter-nally, the duration of egg retention before egglaying can be increased until functional live bear-ing is achieved.67,78,79 Live bearing is hypothesizedto evolve when the associated benefits, such asincreased offspring quality or survival, outweighthe costs of reduced female fecundity or reducedlocomotor performance during pregnancy.73,80,81

A further elaboration on the theme of live bear-

ing is the evolution of substantial postfertilizationmaternal provisioning of embryos during gesta-tion (matrotrophy). The specific means by which

matrotrophy has evolved in different groups arediverse12 and include (1) consumption of invi-able, aborted, or unfertilized ova (i.e., nurse eggs)or, in some rare cases, intrauterine cannibalism of sibling embryos;46,82,83 (2) the ingestion of mater-nal secretions (histophagy) or other body parts;84

and (3) placentation, an intimate fusion of mater-

nal and fetal tissue for nutrition and physiologicalexchange.18 The generalized scenario for the evo-lution of reproductive modes depicted in Figure 4captures much of the diversity present across theanimal kingdom allowing for generalizations tobe made, yet at the same time we recognize itssimplicity and the diversity within groups that itconceals.

Spawning (ovuliparity) During broadcast spawning, multiple individualssynchronouslyexpelgametes intothe water column.Fertilization success is dependent on a multitude of environmental and biotic factors. This reproduc-tive mode is likely ancestral in animals66,73,85 andcan be found in aquatically breeding species, suchas fish and marine invertebrates.1 The nonlocal-ized nature of fertilization and widely dispersingplanktonic larvae limit further interaction with kinand thus preclude parental investment and siblingcompetition.1,86 However, fertilization itself is rife

with sexual conflict.1,85,87–92Eggs are larger and more costly to produce than

sperm. As a result, sperm are produced in far



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greater abundance than eggs, making fertilizationa rate-limiting step for male fitness and result-ing in intense sperm competition.93 The free-for-all breeding system in which sperm and eggs of numerous individuals are released simultaneously imposes intense selection on sperm being able toquickly achieve fertilization. Selection for rapid fer-tilization increases the risk of multiple fertilizations(polyspermy), which is often lethal94 and imposesa cost on both sperm and eggs. This intense spermcompetition in turn imposes selection on eggs toreduce the rate at which sperm are able to penetrateand to mount rapid barriers to polyspermy onceone sperm has penetrated the egg. Each of thesepoints has been demonstrated empirically in the seaurchin and other marine broadcast spawners. Rates

of polyspermy are often very high and are observedeven under conditions of sperm limitation whenoverall fertilization rates are less than 50%.88 Com-parative study within and among urchin species hasdemonstrated that individuals and species that haveeggs capable of being fertilized at low sperm concen-trations are more susceptible to polyspermy, whilethose that require high sperm concentration for fer-tilization are moreresistant to polyspermy.91 Finally,genes that code for proteins involved in fertiliza-tion and gamete recognition are among the fastestevolving of all genes89,90,92,95–98 and exhibit den-sity and frequency-dependent selection.90 Levitanand Ferrell90 demonstrated that the sperm bind-ing genotype of the urchin Strongylocentrotus fran-ciscanus influences reproductive success; commongenotypes are selected at low population densities,facilitating fertilization. At high population den-sities, sperm competition and sexual conflict areintensified, causing rare genotypes to be favored.This combination of rapid evolution and density-

dependent and frequency-dependent selection is asignature of the arms race associated with interge-nomic conflict.

In other aquatic and terrestrial organisms, malesand females form a mating embrace or union (e.g.,amplexus in frogs), with sperm and eggs releasedsynchronously. Although fertilization is still exter-nal, the physical contact and proximity of gameterelease presumably increase the chance of successfulfertilization for both parties while providing somemeasure of paternity assurance. Nonetheless, mul-tiple mating and sperm competition can occur insuch species by means of mating aggregations in

which multiple males swarm a lone female,99 sneak copulations,100,101 or clutch piracy.102 Some speciesexhibit alternative reproductive strategies, such asthose involving males that look diminutiveor mimic

females facilitating sneak copulations at the expense

of the more common courting males.

100,101

In thefrog Crinia georgiana, over 50% of matings involvemultiple males. Such pairings result in significantly reduced fertilization success (68% of eggs fertilizedvs. 96% in single male–female pairings), thus rep-resenting a significant cost to females.99 This reduc-tion in efficiencyof sperm transfer likelyresults fromphysical struggles among males. It is also a signatureof the ongoing conflict between males and females.

Egg laying (oviparity)

Oviparity is characterized by internal fertilizationwith a short period of embryonic developmentwithin the mother, after which eggs are laid. Devel-opment is completed, and hatching happens in theexternal environment. Birds, crocodilians, turtles,and monotremes exhibit this reproductive modeexclusively, as do the majority of arthropods, lizards

and snakes, and some fish. The evolution of inter-nal fertilization by means of copulation opens new arenas for sexual conflict. Although the benefits of polyandry (females mating with multiple males) arewidespread,103–105 males generallyhave more to gainfrom high mating rates than do females,31,106,107

which is predicted to lead to sexual conflict overcontrol of mating. The evolution of internal fer-tilization is associated with the rise of courtshipand increased opportunity for precopulatory femalechoice106,108 but also male morphological adapta-tions for control of mating, including large size,grasping structures, and elaborate copulatory organmorphology.53,109–112 Such male adaptations can

leadto female defensive counteradaptations.53,110,112This conflict over which sex controls copulation isclearly illustrated in water striders, where matingstruggles impose costs on females.113,114 The evo-lution of elaborate grasping hooks in the males of some species is matched by the correlated evolu-tionof antigrasping structuresin females.53 Bedbugsexhibit an extreme case of sexual conflict in the formof traumatic insemination by means of a piercingintromittent organ that bypasses the normal repro-ductive system. Such matings pose significant coststo females in the form of reduced longevity with noapparent compensatory benefits such as increased



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fecundity.111 More generally, thephysical act of mat-ing and internal insemination can be injurious tofemales.115,116

The evolution of internal fertilization provides

opportunity for cryptic female choice or post-

copulatory sexual selection by means of selectivesperm usage, dumping, and storage.117–122 As spermand other seminal fluids are now deposited inter-nally, there is the potential for sexually antagonisticevolution over control of female mating behaviorand remating rate by such varied means as cop-ulatory plugs,123 seminal proteins affecting femalebehavior,124 and sperm storage and use.125,126 Malesbenefit when females bear their (and only their)offspring and produce more than what is optimalfrom a female perspective. In Drosophila, acces-

sory gland proteins contained in the ejaculate havebeen found to alter female behavior by reduc-ing female willingness to remate with other males,increasing female egg production thereby poten-tially enhancing male fitness, and imposing a sur-vival cost on females.124,127–129 Furthermore, theseproteins, along with putative receptors expressed inthe female reproductive tract,130 exhibit extremely rapid evolution, positive selection, and divergenceamong closely related species, which is consistentwith a history of intense sexual conflict.92,130–132

The contact between parent and offspring duringthe narrow time window between fertilization andwhen eggs are laid potentially creates a new venuefor conflict, although it is likely to be limited. Inits incipient stages, parent–offspring conflict may be as subtle as offspring-derived hormones leachingacross a semipermeable egg shell and influencingmaternal physiology (for example, by slightly pro-longing gestation).133 The duration of egg retentionbefore laying varies taxonomically, although most

reptiles retain developing eggs in utero for aboutone-third of embryogenesis.78,134 Radder et al.135

experimentally manipulated laying date in a scincidlizard and demonstrated that the retention of devel-oping eggs in utero for longer periods enhancedposthatching offspring phenotypes (hatching suc-cess, size, and running speed). Since egg gestationcan be costly in lizards,136 it is possible that motherand offspring differ in optimal laying date. If bothpartiesexert an influence over this trait, then conflictmay result. The lizard Lacerta vivipara is remark-able for exhibiting both oviparous and viviparouspopulations. Hybridization experiments between

these interfertile populations indicate that the dura-tion of egg retention is controlled by the mater-nal genotype,137 suggesting limited opportunity forconflict over this trait.

Live bearing (lecithotrophic viviparity) Lecithotrophic live bearers fully provision eggsbefore fertilization and then retain the develop-ing embryos inside the mother for the duration of gestation.19,69 This reproductive mode has evolvedover 100 times in lizards and snakes, in at least 14groups of fish, and several times in sharks and rays(reviewed in Blackburn).17

In lecithotrophs, sexual conflict is expected in thesame arenas as for oviparous taxa. Malesand femalespotentially have different fitness optima for whether

to mate, frequency of mating, and sperm usage (i.e.,fertilization), which has led to a variety of adapta-tions and counteradaptations.138–141 Because mostnutrients are apportioned before fertilization,19,142

opportunities for offspring to extract additionalparental investment are limited,143 putting a cap onboth parent–offspring and sibling conflict. Likewise,

there is likely to be limited selection for postfertiliza-tion screening of offspring (i.e., selective abortion)on the basis of offspring quality or genetic compati-bility with the mother (or father in the case of male-brooding pipefish and seahorses).142 First, becausemostnutritional investment is madebefore fertiliza-tion, this investment would be squandered by selec-tively aborting offspring, unless the parent is able toreabsorb nutrients from aborted embryos.144 Sec-ondly, brooding parents may lack a mechanism forassessing offspring quality. Stillbirth145 and broodreduction146 have been observed in lecithotrophsbut may be due to exogenous factors or geneticdefects in the embryos rather than selective abor-

tion to increase parental fitness.147 For example,in the lecithotrophic mosquito fish (Gambusia affinis ), females abort many offspring when they encounter environments where there is anaerobicdecay of sediments, perhaps because of the releaseof hydrogen sulfide into the water column (D.N.R.,personal observation). Mukherjee et al.145 observedthat pregnant females of Gambusia holbrooki pro-duced on average 14% stillbirths when exposedto the visual cues of a predator (2% for controlfemales). Presumably, such events are the productof maternal physiology, rather than the propertiesof the aborted offspring.



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The duration of brood retention may be onemanifestation of maternal–fetal conflict if there isa tradeoff between maternal and offspring fitness,and this trait is not entirely under maternal con-trol. Female Trinidadian guppies shown modelsof pike cichlid and chemical cues of injured gup-pies gave birth earlier than control females.148 It isplausible that such a response is adaptive for preg-nant females given the well-established locomotorcosts of pregnancy and subsequent reduction inescape performance.19,149 However, having a shorterbrood time negatively affected offspring swimmingperformance,148 suggesting there may be divergencein optimal brood retention time between mothersand offspring. The nature of tradeoffs between thefitness of a mother and her offspring may change

with age. Early in life, mothers may favor them-selves when any conflicts of interest arise, whereaslater in life they may favor the interests of their off-spring as their own residual reproductive value hasdeclined.9,42

Live bearing with matrotrophy (matrotrophic viviparity) Matrotrophicviviparityischaracterizedbylivebear-ing with maternal provisioning of offspring dur-ing gestation. The means by which provisioning

occurs varies taxonomically,12,69 but the result isthe same—significantly expanded scope for sexual,parent–offspring, and sibling conflict in multiplenew arenas.12,39,43,49,50

Sexual conflict. The apposition of maternaland fetal tissues that characterizes matrotrophicviviparity is predicted to increase the impor-tance of immunological and conflict-mediatedgenomic compatibility between mother and devel-oping offspring.150,151 Maternal–fetal mismatch

at immune-recognition loci or those that gov-ern resource transfer can impose costs, such asreduced female fecundity, and may favor multi-ple mating and postcopulatory means of selectingcompatible sperm or offspring.105 The viviparity-driven conflict hypothesis predicts that theevolution of matrotrophic viviparity creates post-fertilization arenas of conflict that are absentin egg-laying species,12,152 increasing the impor-tance and opportunity for postcopulatory sexualselection and even driving the correlated evolu-tion of male sexually selected traits.105,143,152,153

Specifically, matrotrophic viviparity is predicted

to drive a shift from precopulatory mate choice(based on male phenotypes such as size, sec-ondary sexual characteristics, or mating displays)toward postcopulatory mechanisms of mate or off-spring choice105,150,151 by such means as spermcompetition, sperm selection, or postfertilizationselection of embryos.119–121,154–157 Furthermore, inmatrotrophic species, a low initial investment inembryos with subsequent nutritional investmentspread across gestation may make postfertilizationscreening for genetic quality more profitable andmechanistically feasible compared to lecithotrophs.Females may, theoretically, fertilize embryos withsperm derived from multiple males with selectivescreening (the progeny-choice model) for geneticcompatibility, offspring viability, offspring quality,

uniform offspring size, or sex ratio.120,150,151,158–161This cryptic female choice can be viewed as anextreme form of differential resource allocation onthe basis of physiological or genetic interactionbetween the maternal reproductive tract and off-spring genotype.162

There is accumulating evidence that polyan-drous females show an increase in embryo via-bility compared to those that have access to asingle mate, even after controlling for matingfrequency between treatments.104 This is gener-ally regarded as evidence in favor of the geneticincompatibility hypothesis.104,163 In humans, up to75% of embryos never reach full term.43,164 Mam-malian species with promiscuous mating systemsexhibit significantly lower rates of early repro-ductive failure than species with more monoga-mous mating systems, which is congruent with theimportance of the role of polyandry in compen-sating for genetic incompatibility.157 Likewise, inthe placental fish Heterandria formosa, polyandry

was hugely significant in increasing the proba-bility of pregnancy; specifically, 37% of femalespaired with a single male produced offspring, 71%produced offspring when paired with two males,and 89% with four males.165 Empirical work inmammals,166 lizards,117 birds,119 andfish167 demon-strates the effectiveness of postcopulatory choice inbiasing paternity in ways that maximize maternalfitness. Comparative and experimental examina-tion of the interaction between polyandry, repro-ductive mode, rate of reproductive failure, andembryo viability may be a fruitful avenue of futureresearch.



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Although aborting embryos may sometimesincrease a female’s fitness (see above discussionon differential allocation, but also owing to poorenvironmental conditions, developmental abnor-mality, or health risk), offspring and paternal allelesexpressed in offspring should favor staying alive.Developing offspring may overproduce hormonesso as to advertise their condition and hence influ-ence a mother’s decision about whether to abort.43

Control over such “decisions” may be an area of parent–offspring conflict with different forms of resolution in thevarious taxonomic groups in whichplacentation has evolved. In placental fish, moth-ers appear tethered to offspring and are unable toabort embryos and reabsorb nutrients even if envi-ronmental conditions are such that this would be

advantageous.168–170 In a placental skink a higherrate of stillbirth was observed under low-resourcetreatments, and parental cannibalism of abortedembryos increased.171 In several rodent species, theBruce effect is a tendency for pregnant femalesexposed to the scent (pheromones) of an unfa-miliar male to terminate pregnancy by blockingimplantation or, in some species, aborting postim-plantation offspring.171–173 Females then becomereceptive to remating, giving considerable advan-tage to the incoming territorial male. The adaptivevalue of such a swift abortive response is not entirely clear in regard to all players, but it is likely a stablestate that has been molded by conflict. If unableto avoid unfamiliar males,174 mothers may be cut-ting their losses early, thereby avoiding unnecessary investment175 since offspring brought to term arelikelyto be killedby thenewlyestablishedmale.Suchinfanticide is a common occurrence in many mam-malian species ranging from mice to lions.176,177

Females employ a number of strategies to avoid

infanticide, one of which is mating with multiplemales, thereby making it difficult for males to ascer-tain paternity (reviewed in Ebensperger).176

In mammals, female promiscuity is wide-spread,178 yet variation among species allows forinterspecific tests of how mating system influencesthe potential for sexual conflict. Comparative analyses in mammals reveal that polygamy is associatedwith larger testes179–183 and higher ejaculate quality,as judged by higher sperm counts and motility.184

Comparing the phenotypic response to selection inexperimental lines maintained with either polyg-amous or monogamous breeding has providedpowerful empirical tests of conflict theory that

complement these comparative studies. After 12generations, male house mice derived from polyg-amous treatments produced ejaculates with moresperm that had greater motility.185 Competitive fer-tilizations between males from the monogamouslines (which had experienced a history of relaxedselection on sperm competitiveness) and polyg-amous lines revealed a significant paternity biasin favor of sires derived from the polygamouslines.185 These patterns are congruent with numer-ous comparative and experimental evolutionstudiesin insects that characterize the importance of mat-ing system in the evolution of testis characteristics,sperm competition, and male and female reproduc-tive traits.186–191

Parent–offspring conflict. Matrotrophic vivipar-ity creates new opportunities for parent–offspringconflict over offspring rate of resource acquisi-tion, fetal growth rate, and birth size.12,43 Con-verging lines of evidence convincingly argue thatoffspring genotype can influence each of thesetraits.12,20,22,43,192–194 The placenta, which medi-ates resource transfer between mother and off-spring, is seen as a focal point for parent–offspringconflict. Crespi and Semeniuk 12 hypothesize that

internal fertilization potentially provides develop-ing offspring a foothold from which they beginto influence their own provisioning. In some lin-eages, this entry ignites a repeated cycle of adap-tation and counteradaptation in fetal and mater-nal tissues involved in resource transfer that drivesthe evolution of placentation (i.e., a self-reinforcingarms race). One piece of proposed evidence forthis hypothesis is the multiple independent ori-gins of matrotrophic viviparity by diverse meansin different taxonomic groups. If the placenta

is broadly defined as an apposition of mater-nal and fetal tissue specialized for the transfer of nutrients to sustain the physiology of develop-ing embryos, then such an organ has evolved notonly in mammals18,195,196 but also in fish,19,70,197

sharks and rays,71 reptiles,198–200 and many groupsof invertebrates.201–203 Furthermore, such organshave often evolved multiple times within each of these groups.17,73 The striking interspecific diver-sity of placental physiology and morphology is asecond argument for conflict; the mammalian pla-centa has been described as the most phenotypi-cally variable of all organs, despite its apparently conserved function of resource transfer.12,18,204



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There is further evidence of maternal–fetal antago-nism at the placental interface as manifest throughgenetics, physiology, and morphology (reviewedin Crespi and Semeniuk).12 A positive associationbetween placental complexity and maternal invest-ment is evident in mammals, where more complex,elaborate, invasive, or interdigitated placenta areassociated with faster rates of nutrient transfer tooffspring during gestation.205,206 Finally, evidencehas accrued for rapid evolution and positive selec-tion on embryonic and maternal genes expressedin the placenta or other maternal genes that inter-act with the fetus.12,207 Together, this evidence sug-gests that placentas are the battlefront between theacquisition of resources by theembryoand maternalcontrol of allocation.

Genomic imprinting (offspring genes that aredifferentially expressed according to their parentof origin) allows for sexual conflict over offspringresource use to play out within theoffspring’s body.5

In humans and mice, fewer than 1% of genes exhibitthis parent-of-origin expression pattern.208–210 Thatthis phenomena occur at all is peculiar becausespecies that exhibit imprinting are not protectedfrom deleterious recessive mutations at such loci.Furthermore, imprinted loci appear susceptible toderegulation and mismatch and, as a consequence,are associated with a surprising number of growthdisorders and diseases.209,211–213 Owing to theseapparent disadvantages, the origin and mainte-nance of genomic imprinting demand explanation.The conflict theory developed by David Haig andcolleagues63,214–216 posits that differential expres-sion of maternally and paternally inherited allelescan be favored when such alleles affect the fitnessof their parents via effects on offspring growth andinteractions with kin. When one sex is the primary

provider for offspring (as is the case with femalepregnancy in mammals), males and females havedifferent fitness optima with respect to net offspringresource acquisition over the course of develop-ment. For males, there is often no guarantee of con-tinued offspring production with the same female.Thus, male fitness tends to increase when his off-spring are able to acquire a larger share of invest-ment than is optimal for the mother to provide.This inequality between male and female optimatranslates to males benefiting by siring more aggres-sive offspring that are able to obtain a greater shareof maternal resources, whereas females benefit by

having more cooperative and restrained offspring.In its simplest incarnation, paternally derived allelesthat promote offspring growth during developmenthave been selected for overexpression at the sametime that the maternally inherited copy is selected

for under expression. This tug of war over net geneexpression levels (played out within the offspring’sbody) has been likened to a contest in which the“loudest voice prevails”; the resulting evolutionar-ily stable equilibrium is the circumstance in whichthe allele inherited from one sex is silenced andthat of the other sex is expressed at its optimallevel.214,216

The conflict theory makes predictions that can betested with empirical data, namely the phylogeneticdistributionof imprinting as a function of reproduc-

tive mode and mating system, the tissues in whichimprinted genes are likely to be expressed, and, to acertain extent, the function of such genes and whichparental copy is likely to be silenced. Specifically,the theory predicts paternally expressed loci shouldbe growth promoting and favor selfishness, whilematernally expressed loci are expected to be growthretarding and favor cooperativeness. Because of theprolonged and intimate physiological interactionbetween mother and offspring, the presence of pla-centation provides perhaps the strongest and clear-est arena in which alleles expressed in offspring areable to manipulate levels of maternal investment.12

Thus, according to the kinship theory, reproductivemode is likely to be a large determinant of the poten-tial for conflict and hence selection for genomicimprinting.217–219 Imprinting has been conclusively demonstrated in mammals and angiosperm plantsin association with the placenta and endosperm—tissues that mediate resource transfer betweenmother and offspring.213,215,216,220,221 Several mam-

malian imprinted genes, most notably insulin-likegrowth-factor two (IGF2) and insulin-like growth-factor two receptor (IGF2R), exhibit patterns thataccord well with the conflict theory.216 A num-ber of other intriguing cases have been uncoveredin which imprinted genes contribute to huddlingbehavior,222 language development,223,224 maternalcare,225 and the social brain,210,211,226 notably allcases that involve family interactions and the poten-tial to acquire parental investment. The conflictor kinship theory of imprinting has been seam-lessly expanded to include parent-of-origin spe-cific expression in these tissues or development



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periods and their often indirect effects on parentalfitness.214,219,227–233 In baby mammals, behavior isused to solicit maternal investment and governssocial interactions (i.e., cooperativeness vs. selfish-ness) with both themother andsiblings; as theorganthat generates this social behavior, the brain may take on a role analogous to the placenta such that,even here, gene expression levels may be a target of selection in the context of family conflict.

Experimental evidence of parent–offspring con-flict at the placental interface, the role of genomicimprinting, and the potential for conflict to gen-erate phenotypic mismatch is manifest in recip-rocal crosses between sister species of deer mice(genus Peromyscus ) that differ in mating system.20

Peromyscus polionotus is primarily monogamous,

whereas P. maniculatus females frequently matewith multiple males.20,216,234,235 Crosses betweenmale P. maniculatus and female P. polionotus resultin pathologically large offspring, massive placenta,and developmental abnormality,20,236,237 whereasthe reciprocal cross produces viable but growth-retarded offspring. Imprinted loci contribute sub-stantially to these differences.20,21,237 Asymmetricdevelopmental effects are also observed in recip-rocal crosses between lions and tigers. A male lioncrossed with a female tiger produces offspring thatgrow to twice the size of either parent, while a maletiger crossed with a female lion has offspring slightly smaller than either parent.20,238 Lions live in pridesand females frequently mate with multiple males,239

resulting in high levels of extra-group paternity insome populations.240 In contrast, tigers are typically solitary with large ranges and may have less oppor-tunity for multimale mating during a single breed-ing season. A parent–offspring conflict perspectiveparsimoniously accounts for these phenotypic pat-

terns of offspring growth: populations or specieswith frequent multiple mating have experienced ahistory of intense intrafamilial conflict, resultingin selection for high expression levels of growth-promoting paternal alleles, which are matched by equally defensive growth-retarding maternal alle-les (or the silencing of maternal copies of growth-promoting alleles). Conversely, the genetic interestsof parents and offspring are more closely alignedin relatively monogamous populations or species,resulting in relaxed selection. In both mating sys-tems, paternal and offspring aggressiveness andmaternal restraint have coevolved and are thus

matched, resulting in normal offspring phenotypesfrom intraspecific crosses. However, interspecifichybrids result in a mismatch where an aggressivegrowth-promoting paternal genome is paired witha permissive maternal line, resulting, at least inPeromyscus , in pathologically large offspring, or viceversa in the reciprocal cross (for another example of this phenomenon in Arabidopsis plants, see Willi,241

Haig,242 and Crespi and Nosil).243

Haig,43 in his seminal paper on genetic con-flicts during human pregnancy, argued thatconflict explains several otherwise puzzling orwasteful aspects of human pregnancy. For exam-ple, preeclampsia, arterial remodeling during tro-phoblast invasion of the uterine wall, and excessivehormone production by the human placenta can

all be understood as phenotypic manifestations of parent–offspring conflict.12,43,244–246 Placental hor-mones produced by offspring and released into thematernal bloodstream are able to act on maternalreceptors and are thus prime candidates for theexpression of parent–offspring conflict.43,44,247 Fur-thermore, the conflict perspective may explain why male offspring are more susceptible to preterm birththan females.248 If the aggressiveness of resourceextraction rate varies among offspring, and themother is partially in control of birth timing, thenfaster growing fetuses may trigger earlier partu-rition. A mother could “punish” aggressive off-spring by giving birth early so as to avoid, or atleast minimize, the costs they impose. In sexually dimorphic species, including humans, males andfemales may have different growth strategies thatbegin before birth. A recent review on this topicindicatesthatmalefetuses employ a relatively invari-ant growth maximization strategy, whereas femalefetuses adjust gene expression and growth rates in

response to varying maternal environments.249 Amale fetus’ “grow fast no matter what” strategy may put him in greater conflict with maternal interests,especially in resource-limited environments, andthis may make males more susceptible to a hostof adverse pregnancy outcomes, including pretermbirth.

Sibling conflict. Matrotrophic viviparity in com-bination with the production of mixed paternity litters creates new venues for sibling conflict aswell. The diminished relatedness of offspring co-inhabiting the body of a gestating female is expected



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to increase competition for maternal resourcesand/or reduce cooperativeness in extracting mater-nal investment.44,250 Comparative tests across mam-mals are consistent with a prominent role forsibling competition in driving patterns of offspringgrowth rate. Offspring growth rate during gesta-tion is positively correlated with testis mass (a reli-able proxy for mating system).182 This suggeststhat an increase in familial conflict has selectedfor aggressive offspring able to garner maternalresources at faster rates.251–253 Placental fish of thefamily Poeciliidae show patterns of offspring size atbirth and postnatal growth rates that are suggestiveof sibling competition.165,254 Female Heterandria

formosa allowed to mate with four males had off-spring with longer maturation times than monan-

drous females. Further, offspring size at birthdecreased over time for females assigned to a treat-ment that resulted in low within-brood geneticrelatedness; in contrast, birth size stayed constantfor females with high within-brood relatedness.165

Both patterns are consistent with negative pheno-typic effects for offspring, resulting from reducedcooperativeness in extracting maternal investment.

If offspring differ in competitive ability or growthstrategies, then we might expect higher variancein offspring size and presumably offspring fit-ness at birth than is optimal from the maternalperspective.160 For example, in Soay sheep, femalelambs with a male cotwin had reduced birth weightrelative to those with a female cotwin, and thesedifferences in size had long-term consequences onsurvival and reproduction.255 Furthermore, siblingsmay interact in utero in more subtle ways, even with-out direct competition over maternal resources.256

In rodents, the sex of neighboring fetuses affectsa variety of morphological, behavioral, and life-

historical traits in siblings. For example, femalerodents gestated between two male siblings exhibitmore masculine morphology, higher testosteronelevels, and exhibit lower fecundity.257,258 Theselong-lasting effects are driven by sex-specific steroid hor-mone leakage across fetal membranes.259

The tradeoff between offspring size and num-ber may be particularly important in viviparoustaxa and provide a venue for conflict. Mothers havelimited space to house gestating offspring; there-fore, producing larger offspring necessarily meansproducing fewer offspring. The consequences of a tradeoff between number and size of offspring

will differ between parents and offspring.57,260 Off-spring benefit from larger size and hence fewer sib-lings, but mothers benefit from the production of more offspring.13–15 Matrotrophic viviparity creates

a venue in which siblings directly compete with each

other for limited maternal investment, often in aconfined space. Intrauterine cannibalism—the con-sumption of sibling ovaor embryos—may representan extreme manifestation of this conflict. In speciesin which intrauterine cannibalism is a regular phe-nomenon, including some sharks, teleost fish, andamphibians,46,261–265 offspring actively control can-nibalism levels and may be able to winnow broodsize to the level that maximizes their inclusivefitness12 at the expense of their parent’s optimum.Lamnoid sharks display two contrasting reproduc-

tive strategies. In most species, 2–9 fetuses coexist ineach uterus where they consume trophic eggs ovu-lated by the mother, gestation lasts 12–15 months,and typical birth sizes are 40–70 cm. In the secondstrategy (documented only in the sand tiger shark),the largest fetus in each uterus actively cannibal-izes all siblings before turning to a diet of trophiceggs. This results in the birth of a single 1-m–long predatory neonate from each of two uterinecompartments.47

Postembryonic parental care and the potential for family conflict Posthatching or postnatal parental care cuts acrossour reproductive mode classification scheme andallows for continued interaction between parents,siblings, and other kin after embryonic develop-ment is complete, thus creating new venues for con-flict. The addition of behavioral interactions amongmates, between parents and offspring, or amongoffspring can be associated with behaviors that

benefit one party at the expense of others. Exam-ples of posthatching parental care in species withexternal fertilization include nest guarding in themajority of freshwater fish,72,266 mouth brooding incichlids,267 andthetransportandfeedingoftadpolesin poison dart frogs.268 In nest-guarding fish, bothfilial cannibalism (parents eating offspring) and sib-ling cannibalism occurs (reviewed in Smith andReay).269 There is support for the hypothesis thatparents consume offspring when this act maximizestheir lifetime reproductive success.270 For exam-ple, in mouth brooding male cardinal fish, phys-ical condition decreased with the advance of the



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breeding season and so did the frequency of broodcannibalism.271

In species with internal fertilization and egg lay-ing, examples of parental care include feeding of nestlings in birds,2 nest excavation and protec-tion of young in crocodilians,272 and nursing inmonotremes.273 Finally, some viviparous taxa pro-vide extensive postnatal care, most notably lacta-tion in mammals.34 Mock and Parker2 and Roulinand Dreiss50 provide an in-depth treatment of sibling competition primarily in birds, and Hud-son and Trillmich49 do the same for mammals. If resource availability during the breeding season isunpredictable at the outset, then parents may pro-duce more offspring than they can normally rear,enabling them to capitalize on abundant resource

years and have higher fecundity.2,48,274,275 If, how-ever, resources are scarce, marginal individuals withlow residual reproductive value will be selectively eliminated through sibling competition, resultinginthe productionof fewer, high-quality offspring.50,275

Theory indicates that the threshold for siblicideis lower than for infanticide.276 Functionally, thismight mean that parents and dominant offspringhave congruent interests in brood reduction (i.e.,siblicide) when resources are very scarce, but if resources are slightly more abundant, the domi-nant sibling will derive greater benefit from killinga sibling than parents (reviewed in Roulin andDreiss),50 potentially resulting in parent–offspringconflict.

Sibling competition for food and space can beintense in birds, and siblicide is a regular featurein some species.2,277,278 Several factors have beenidentified that determine whether sibling compe-tition can occur and its form and intensity. Inprecocial species that are able to feed themselves

(i.e., chickens), scramble competition for availablefood resources with no parental involvement isthe rule, and sibling competition is predicted tobe less intense.279 In altricial species, the confinedspace of a nest, hatching asynchrony, developmentof dominance hierarchies, and reliance on parentalfeeding lead to higher degrees of competition thatcan culminate in obligate siblicide.50,278–280 Further-more, as is the case in many other manifestationsof conflict, genetic relatedness among siblings candetermine the intensity of conflict. Comparativeanalyses across birds have demonstrated that loud-ness of begging behavior increases with levels of extra-pair paternity.281 Similarly in the barn swal-

low, higher levels of begging are observed whennestling relatedness is reduced.282 Finally, compar-ative studies reveal that nestling growth rate tendsto increase in association with the level of multiplepaternity.283

Parent–offspring conflict over resource provi-sioning may be expected in the form of beggingbehavior, where offspring may not be honest sig-nalers of need but instead attempt to solicit addi-tional parental investment, presumably at a costto future parental reproductive potential.9 In hisoriginal formulation of parent–offspring conflict,Trivers9 focused primarily on the overt behav-ioral manifestations associated with offspring beg-ging behavior/weaning date. Several competingmodels have been developed to account for beg-

ging behavior (reviewed in Wells),45 including (1)blackmail, (2) scramble competition between off-spring, (3) honest signaling of nutritional need,and (4) honest signaling of quality. Each modelhas garnered support in different taxa or ecologi-cal situations,45,284–288 and distinguishing manipu-lation from honest signaling remains an empiricalchallenge.45,287

Parent–offspring conflict can extend to offspringdispersal behavior from the parental territory. Amother’s inclusive fitness is often maximized whenoffspring disperse from thenatal territory and hencecompete more intensely with less-related kin thanwith siblings and herself. Yet, dispersal from a natalterritory is risky because traveling through unchar-tered territories in search of a suitable habitat canlead to increased mortality. Theory predicts thatthe optimal dispersal distance is often shorter fromthe offspring’s than parent’s perspective.289,290 Theactual dispersal distance is a function of who hasgreater control over the process. In plants, dispersal

is presumably under maternal control since the seedcoatandfruitbodiesthatcontaintheadaptationsfordispersal are made of maternal tissues and are there-fore a product of the maternal genome.290 In many animals the situation is more complex because dis-persal is the product of behavioral interaction andindividual personality.291,292 Thus, we might expectconflict over eviction in territorial mammals orbirds, maternal effects on offspring dispersal behav-ior, and the evolution of genomic imprinting indispersal-relatedtraits. In somemammals and birds,offspring are expelled fromparentalterritories.293 Innewly fledged Siberian jays, there is sibling rivalry over delayed dispersal, with dominant brood mates



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staying in the natal territory for 1–3 years andsubordinate brood mates dispersingimmediately.294

This suggests that there are benefits of staying inthe natal territory that are worth fighting for.294,295

In side-blotched lizards, sire genotype and mater-nal effects interact to determine offspring disper-sal distance296 and, in the common lizard (Lacerta vivipara ), maternal plasma corticosterone levels,whilegestating affects offspring dispersal strategy.297

Finally, in mice, the imprinted gene Nesp55 ismaternally expressed in the brain, and deletion of this gene results in abnormal reactivity to novelenvironments. It has been suggested that, in thiscontext, exploratory and risk-taking behavior may represent targets of differential selection on thematernal and paternal genome, which can lead to

imprinting.298,299Biparental care of offspring also creates new

venues for conflicts between parents. As the sex thatlays eggs or gives birth, females are assured of mater-nity, yet the same is not true for males. A surprisinginsight derived from molecular paternity analyses isthe high levels of polyandry among socially monog-amous species.300,301 Polyandry is widespread(fish,302 reptiles,303 birds,304 mammals),178,182 anddespite costs,35,39 polyandrous females often receivenet fitness advantage relative to monogamous coun-terparts, for example, through higher fecundity,103

an increase in embryo viability,104 or enhanced off-spring quality.104,166,305 A cuckolded male providinginvestment in offspring of another father isn’t con-tributing to his fitness and thus males are expectedto employ strategies such as mate guarding that seek to minimize this informational asymmetry, enhancepaternity assurance, and prevent misplaced invest-ment. Postcopulatory mate guarding is commonamong birds and mammals.306–309 Further, consis-

tent with this prediction, male birds provide a levelof care that is commensurate with the relative levelof assurance they have that the offspring they arecaring for are their own.310,311

Future directions

Comparative variation in reproductive mode pro-vides the raw material to test targeted predictionsregarding the appearance and phenotypic manife-stations of conflict. For example, the viviparity-driven conflict hypothesis predicts that theevolution of matrotrophic viviparity from ovipar-ity will create new arenas of evolutionary conflict

and drive phenotypic evolution.105,143,152,312 Oneprediction is that viviparous females will exhibitan increased reliance on multiple-mating and post-copulatory means of choosing compatible sires and

offspring.143 Another prediction is that rates of

reproductive failure and embryo abortion may behigher for viviparous species, particularly whenfemales have access to limited mates.165 Further-more, the viviparity-driven conflict hypothe-sis makes predictions at the macroevolutionary level regarding the speed at which reproduc-tive incompatibilities evolve within species thatdiffer in reproductive mode.152 The hypothesispredicts an increase in postzygotic reproductiveisolation among viviparous populations, owingto the generation of conflict-mediated genomic

incompatibilities.152,312 Each of these predictionsregarding the phenotypic manifestations of evolu-tionary conflict either requires or can be fruitfully addressed using closely related species that differ inreproductive mode. Thus, continued characteriza-tion of reproductive mode by combining molecularphylogenies with morphological, anatomical, andbehavioral study will prove valuable.

The convergent evolution of reproductive modeacross the tree of life provides opportunity toexamine the repeatability of molecular and pheno-typic evolution owing to family conflict. For exam-ple, there have been multiple independent originsof matrotrophy in live-bearing taxa. Is genomicimprinting found in embryonic tissue involvedin resource acquisition in all such taxa, or only a subset that includes placental mammals? Doesconflict arise in the same arenas and by similarmechanisms in each of the diverse lineages thathave evolved matrotrophy, or is this dependent onlineage-specific factors? Has conflict been resolved

or minimized by similar means in different lineages?Conversely, reproductive diversity and nature’s odd-ities provide opportunities to examine the general-ity of underlying principles.313 In sex role–reversedspecies in which males provide higher levels of parental investment than females, such as pipefishand seahorses, we might expect father–offspringconflict in ways analogous to taxa with primarily prenatal maternal care.66

In this review, we have focused primarily oncataloging the empirical manifestations of con-flict within different categories of reproductivemode. Yet, in addition to being a consequence of



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reproductive mode, family conflict could actually act as a creative force that drives transitions amongstates. For example, sexual conflict over control of mating and fertilization could contribute to the evo-lution of internal fertilization. For males, internalfertilization could be the culmination of intensesperm competition—a form of paternity assurancethat involves depositing sperm as close to eggs asphysically possible.77 Conversely, for females, inter-nal fertilization may allow for postcopulatory arenasof mate and sperm choice—a means by which towrestle back control of reproductive decisions.314

Likewise, once live bearing has evolved, parent–offspring conflict at the maternal–fetal interface hasbeen hypothesized to be a driver of the diverse formsand multiple independent origins of matrotrphy.12

Here, the conflict hypothesis posits that extensivematrotrophy (i.e., placentation) results as a poten-tially nonadaptive by-product of a self-reinforcingarms race between mothers and gestating offspringover control of nutritional provisioning.12 Testingadaptive and conflict hypothesesregarding theselec-tive factors that drive transitions among reproduc-tive mode remains an empirical challenge. Finally,despite numerous instances of convergence in theevolution of more derived reproductive modes,reversals (for example, from live bearing to egglaying) appear to be comparatively rare and fur-ther phylogenetic study or corroborating evidenceis warranted.315,316 What accounts for such patterns?If theevolution of more derived reproductive modesis predictably associated with the rise of new arenasof conflict and associated arms races, species may be entering an alleyway from which it is difficult toreturn.

Conclusion

Family units are defined by their genetic related-ness, mutual dependence, and transfer of invest-ment between players. Even in such tightly knitand interdependent relationships, individuals areexpected to have different fitness optima for traitsthat govern the flow of investment (time orresources) between males and females, parents andoffspring, and among siblings. Following Trivers’9

seminal paper on parent–offspring conflict, therewas a focus on the readily observable behav-ioral manifestations of conflict, for example, sexualconflict over mating rate, parent–offspring con-flict over weaning, and overt sibling competitionbetween nest mates. Subsequently, there has been an

exponential growth in the literature with extensionto realms including sperm–egg interaction, crypticfemale choice, embryo selection via differential allo-cation of resources to offspring, parent–offspringconflict during pregnancy, and intraindividual con-

flict through the evolution of genomic imprint-ing. The idea that reproductive mode determinesthe context and degree to which family mem-bers interact, and thus governs the opportunity for evolutionary conflict (and cooperation), hasbeen apparent from the inception of the concept.Empirical and theoretical studies have fleshed outthe scope and diversity of such conflicts. Conflictis theoretically possible in multiple physical are-nas, over a variety of shared traits, and can resultin a multitude of adaptations and counteradap-

tations through antagonistic selection. Yet, suchconflict is not equally likely to occur in different tax-onomic groups that have different mating systemsand modesof reproduction. Considerationof repro-ductive mode allows for the generation of targetedpredictions regarding the tissues, life history stages,and traits over which conflict is expected. The pri-mary goal of this review is to argue that the physicalarenas where conflict occur, the particular manifes-tations of conflict, and its intensity are determinedby the interaction between reproductive mode andmating system. We have focused on major categoriesof reproductive mode (broadcast spawning, egg lay-ing, live bearing, and live bearing with matrotrophy)and highlighted some of the more theoretically andempirically well-explored manifestations of sexual,parent–offspring, and sibling conflict. One end of thespectrum is definedby broadcast spawners; here,eggs and sperm are released simultaneously into thewater column, and conflict over fertilization in theform of sperm–egg interactions can be very intense;

yet, further parental investment or even interactionbetween family members is unlikely, thus limitingsexual conflict solely to the act of fertilization itself.At the other end of the spectrum, the potential forfamilyconflict reaches itsapex in highlysocialmam-mals, where there is potential for extensive pre- andpostnatalconflict.Wehopethatthisreviewcanserveas a useful framework for organizing the burgeon-ing evidence for conflict, interpreting the pheno-typic manifestations of conflict, and as a catalyst forgenerating predictions on the interaction betweenreproductive mode and the opportunity for conflictthat can be tested with experiments and compara-tive data.



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Acknowledgments

We thank Erol Akçay, Cynthia Dick, Bart Pollux,John Regus, and Will Roberts for stimulating dis-cussion on the topic of evolutionary conflict, andtwo anonymous reviewers for helpful comments on

an earlier draft.

Conflicts of interest

The authors declare no conflicts of interest.

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Annals of the New York Academy of Sciences - Furness Et Al-2015