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R E V I E W A N D

S Y N T H E S I S Eco-evolutionary feedbacks between private and public goods:

evidence from toxic algal blooms

William W. Driscoll,1,2,3*

Jeremiah D. Hackett3 and

Regis Ferriere2,3*

1Department of Ecology, Evolution

and Behavior, University of

Minnesota St. Paul, 5106 MN, USA 2Ecole Normale Sup erieure Institut

de Biologie de l’ENS (IBENS), CNRS

UMR 8197, 46 rue d’Ulm, Paris,

F-75005, USA3Department of Ecology and

Evolutionary Biology University of

Arizona Tucson, 85716 AZ, USA

*Correspondence: E-mail:

[email protected] (or)

[email protected]

Abstract

The importance of ‘eco-evolutionary feedbacks’ in natural systems is currently unclear. Here, we

advance a general hypothesis for a particular class of eco-evolutionary feedbacks with potentially

large, long-lasting impacts in complex ecosystems. These eco-evolutionary feedbacks involve traits

that mediate important interactions with abiotic and biotic features of the environment and a self-

driven reversal of selection as the ecological impact of the trait varies between private (small scale)

and public (large scale). Toxic algal blooms may involve such eco-evolutionary feedbacks due to

the emergence of public goods. We review evidence that toxin production by microalgae may yield

‘privatised’ benefits for individual cells or colonies under pre- and early-bloom conditions; how

ever, the large-scale, ecosystem-level effects of toxicity associated with bloom states yield benefits

that are necessarily ‘public’. Theory predicts that the replacement of private with public goods

may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often

harbor significant genetic and functional diversity: bloom populations may undergo genetic differ-entiation over a scale of days, and even genetically similar lineages may vary widely in toxic

potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting tha

toxic blooms may serve as useful models for eco-evolutionary dynamics in nature. Eco-evolution-

ary feedbacks involving the emergence of a public good may shed new light on the potential for

interactions between ecology and evolution to influence the structure and function of entire

ecosystems.

Keywords

Eco-evolutionary dynamics, eco-evolutionary feedback, multiscale dynamics, public good

sociomicrobiology, toxic algae bloom.

Ecology Letters (2016) 19: 81–97

INTRODUCTION

Interactions between ecological and evolutionary processes

can lead to population- and community-level phenomena that

cannot be understood on the basis of each process operating

in parallel (Fussmann et al. 2007; Schoener 2011). One partic-

ularly intriguing possibility is that ecological and evolutionary

change may feedback to reciprocally influence one another

(Reznick 2013). Such ‘eco-evolutionary feedbacks’ can be

described by using three ingredients: (1) heritable traits that

affect some ecological properties of the system, (2) ecological

modifications that are persistent and strong enough to alter

selection on the traits, and (3) an actual adaptive response of

these traits to the change in selection (Ferriere et al. 2004;

Kokko & Lopez-Sepulcre 2007). We call ‘eco-evolutionary

dynamics’ the dynamics of ecological and evolutionary

variables when such a closed feedback loop operates between

ecological and evolutionary processes (Smallegange &

Coulson 2013).

Over the last 10 years, the development of several model

systems has facilitated direct tests of theoretical models of

eco-evolutionary feedbacks and dynamics (Ellner 2013). How-

ever, the significance of these processes for natural ecosystems

remains unclear due to the relative scarcity of field studies.

(Strauss 2014). In particular, the spatial and temporal scales

of eco-evolutionary feedbacks, and the impact of these effects

on the structure and function of natural ecosystems, remain

largely unknown (De Meester & Pantel 2014). Strauss (2014)

echoed Fussmann et al. (2007) and Schoener (2011) when she

stated, ‘our biggest challenge remains to understand how

often and when eco-

evolutionary dynamics could be expected to have large, long-

lasting impacts in complex field ecosystems’ (Strauss 2014).

This essay explores toxic algal blooms as potential natura

demonstrations of eco-evolutionary feedbacks centred around

the emergence of widely distributed ‘public goods’. We begin

by describing a general hypothesis for a particular class of

eco-evolutionary feedbacks with potentially ‘large, long-lasting

impacts in complex field ecosystems’. Next, we review evi-

dence from the harmful algae literature for eco-evolutionary

feedbacks involving ‘private’ and ‘public’ aspects of toxin pro-

duction. We then provide several (brief) illustrations of the

key elements of this feedback from a broad range of ecologi-

cal systems, including plant and animal communities, as well

as laboratory microbes. We consider the implications of the

lack of obvious terrestrial analogues for toxic algal blooms

both for the existence of these processes, as well as our ability

to detect and measure them over practical timescales. Finally

© 2015 John Wiley & Sons Ltd/CNRS

Ecology Letters, (2016) 19: 81–97 doi: 10.1111/ele.12533


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we highlight major challenges and opportunities within and

beyond the field of toxic algal bloom research.

THE CONCEPT OF EMERGENT PUBLIC GOODS IN

ECO-EVOLUTIONARY FEEDBACKS

Here, we introduce a simple conceptual framework to explain

the role of emergent public goods in eco-evolutionary feed-

backs. We focus on the very simple case of a costly trait

within a polymorphic population that positively influences

direct interactions between individuals and some aspect of

their environment. An eco-evolutionary feedback may arise

when the following conditions are met:

(1) The trait is favoured by natural selection in sparse popula-

tions due to individual-level advantages (‘private good’);

(2) The distribution of benefits extend beyond the level of indi-

viduals due to novel ecological effects of the trait, which

may be triggered by local increases in population density or

other changes in ecological context (positive feedback);

(3) Selection reverts to favour conspecifics that do not bear

the focal trait (‘public good’).(4) The decline of individuals expressing the trait contributes

towards restoring the system to the initial state (‘tragedy

of the commons’).

In this scenario, a trait that primarily impacts direct interac-

tions at the level of individuals shifts to yield ‘public’ benefits

at broader levels (e.g. subpopulations or entire communities).

However, these larger scale (and potentially long-lasting)

benefits may obviate the original, individual-level functions,

ultimately undermining the ‘privatizable’ aspects of the trait.

Because an individualistic trait gives way to a true public

good not by evolutionary change (i.e. the evolution of cooper-

ation), but through ecological change, we call this an emergent

public good, in contrast with an evolved public good. We pre-

sent a graphical representation of this hypothesis in Box 1,

and discuss relationships with established concepts from

evolutionary game theory in Box 2.

EMERGENT PUBLIC GOODS AND ECO-

EVOLUTIONARY FEEDBACKS IN TOXIC ALGAL

BLOOMS

Although humans have known of toxic algal blooms (TABs)

for (at least) hundreds of years, the frequency and severity of

blooms is increasing as a result of anthropogenic nutrient

loading, pollution and climate change (Paerl & Huisman

2009). For our purposes, we operationally define a toxic

bloom as a dramatic increase in the density of one or a few

species of microalgae, at least one of which produces toxins

that negatively impact other members of the native plankton

community. (We are not concerned with non-toxic algae

blooms that are ‘harmful’ as a result of physical properties of

the cells, or due to byproduct effects of extreme densities (e.g.

anoxia).)

Toxic blooms may occur in virtually any aquatic environ

ment with adequate nutrients. The diversity of environments

impacted by TABs is matched by the phylogenetic and ecologi-

cal diversity of the causative organisms themselves: the

prokaryotic cyanobacteria and members of two of the three1

major photosynthetic eukaryotic phyla (alveolata and

stramenopiles) are known to cause toxic blooms. Microalga

toxins are similarly diverse in structure (including cyclic pep-

tides (Jungblut & Neilan 2006), fatty acids, and alkaloids (Van

Dolah 2000)), mode of action (they may attack lipid bilayers

block specific ion channels or mimic neurotransmitters (Van

Dolah 2000)), and deployment (toxins may be retained

intracellularly, injected into targets, or actively secreted).

Several long-held assumptions about blooms and the organ-

isms that cause them are currently being challenged on the

basis of molecular data, microscopic observations, and theo-

retical modelling. Blooms had commonly been viewed as the

result of ‘adaptive strategies’ of entire, genetically homoge-

nous populations (Thornton 2002); however, recent advances

in molecular biology have revealed the surprising genetic and

taxonomic heterogeneity of toxic blooms. Concurrently, a new

appreciation for the sophistication with which individual cells

wield toxins for defensive and offensive purposes has focused

new attention on the cell (rather than population) as an

important ecological agent. Finally, the (still common) distinc

tion between ‘phytoplankton’ and ‘zooplankton’ is increas-

ingly questioned as examples of ‘mixotrophic’ (combining

autotrophy with heterotrophic acquisition of nutrients) species

accumulate (Flynn et al. 2013). Indeed, mixotrophs2 are par-

ticularly well represented among TAB-forming eukaryotes

(Stoecker 1999; Graneli 2006; Burkholder et al. 2008).

Below, we briefly review key aspects of TAB ecology and

evolution through the lens of four key assumptions of the

emergent public goods hypothesis: (1) Toxin production is

advantageous for individual cells (or colonies) under certain

conditions (private good), (2) Increasing toxicity and cell den-

sity result in large-scale ecological changes that further benefit

toxic populations (positive feedback), (3) Benefits extend to

the surprising diversity of genotypes and phenotypes within

the blooming population, including non-toxic, resistant

lineages (public good), and (4) Non-toxic, resistant cells that

benefit from the emergent public good may undermine the

public good (tragedy of the commons).

The benefits of toxin production can be ‘privatized’

We highlight two basic classes of cell-level functions3 of toxic-

ity: ‘defensive’ (grazing deterrent) and ‘offensive’ (assistance in

predation). Both offensive and defensive cell-level functions

have been demonstrated under laboratory conditions for

several important species of toxic microalgae (Table 1).

1We are unaware of toxic unicellular green algae, although the multicellulargenera Ulva and Ulvaria do produce toxic blooms (Nelson et al., 2003).2We follow Flynn et al. (2013) in reserving the term ‘mixotroph’ to refer toorganisms that engulf particulate organic material (phagocytosis), excludinglineages that take up dissolved organic material through osmotrophy, as thislatter group appears to include virtually all autotrophic microalgae.

3Some important microalgal toxins may serve unrelated functions, and nega-tively influence other organisms only as a ‘byproduct’; for example, domoicacid produced by diatoms appears to function as an iron chelator (Rue & Bru-land 2001).


82 W. W. Driscoll et al. Review and Synthesis


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Toxicity as chemical defence: deterring choosey predators

Animal and microbial predators4 exert strong top-down

controls on the standing biomass of primary producers in

most aquatic environments (Cyr & Face 1993; Polis 1999;

Shurin et al. 2006). It is therefore not surprising that, like

their terrestrial counterparts, planktonic algae have evolved

numerous physical, behavioural and chemical defences

against predation. Chemical defences vary considerably inregulation, structure and mode of action, and include the

potent neurotoxins implicated in paralytic and diarrhoetic

shellfish poisoning (Van Dolah 2000). As in terrestrial

plants, many microalgae dynamically regulate toxin produc-

tion in response to specific or general grazing signals,

presumably minimising metabolic/physiological costs (Van

Donk et al. 2011).

Many important predators show a surprising ability to

preferentially avoid, reject or expel toxic prey at the level of

individual cells or colonies: zebra mussels (Vanderploeg et al.

2001), Daphnia (Haney & Lampert 2013), copepods (Teegar-

den 1999), rotifers (Kirk & Gilbert 1992) and unicellular

predators (Strom et al. 2003; Graham & Strom 2010) are all

capable of rejecting toxic prey in mixtures with nontoxic

prey (Table 1). These selective predators may play important

roles in maintaining toxicity within populations by selectively

targeting low-toxicity strains (Teegarden 1999). Furthermore

selective grazing may play a key role in bloom initiation by

favouring toxic lineages over non-toxic competitors

Box 1 A graphical model of emergent public goods through eco-evolutionary feedbacks.

Eco-evolutionary feedbacks consist of three ingredients: (1) heritable traits that affect some ecological properties of the system,

(2) ecological modifications that persist long enough and strongly enough to alter selection on the traits, and (3) an actual

adaptive response of these traits to the change in selection.Multiple related frameworks are available to model these eco-evolutionary dynamics (Dieckmann & Law 1996; Metz et al.

1996; Abrams 2000; Dercole et al. 2002; Hairston et al. 2005; Champagnat et al. 2006; Cortez & Ellner 2010). Eco-evolutionary

modelling highlights the importance of the traits-to-ecology map (the ‘ecology map’, in short), which translates ingredient (i);

and the traits 9 ecology-to-fitness map (the ‘fitness map’, in short), which captures ingredient (ii). Figure 1 schematically illus-

trates how these maps together determine the expected eco-evolutionary equilibrium [or equilibria, and/or more complicated

attractor(s)] in a constant environment.

Figure 2 depicts the interaction between ecological and evolutionary change in the context of emergent public goods. In

Fig 2a – d, the ecology map is S-shaped to indicate the existence of alternative ecological states, such as low vs. high equilibrium

population density, over a range of trait values. The S-shape is meant to capture the existence of ‘tipping points’ (threshold

effects) of high density and/or high toxicity: for a given toxicity (within the appropriate range), the large-scale ecological effects

of sufficiently high density can drive the population from one stable state (e.g. low density) to another stable state (e.g. high

density). This scenario could be realised by positive feedbacks between density and net growth rate, which are generally relevant

to the onset of toxic blooms.

Mean trait value

E c o

l o g i c a l s t a t e

( e .

g .

p

o p u l a t i o n s

i z e )

Figure 1 Ecological and evolutionary ingredients in eco-evolutionary modelling. In this simple depiction, the evolutionary dynamics develop along a

single-trait axis (horizontal) and the ecological dynamics develop along a single state variable (such as population density) axis (vertical). The plain,

thick curve (blue) is the trait-to-ecology map, which represents the equilibrium ecological state as a function of the trait. Vertical (blue) arrows indicate

that the equilibrium is stable at all values of the trait. The dashed, thin curve (red) is (the zero contour of) the trait 9 ecology-to-fitness map (or ‘fitness

map’); it is the locus of trait and population size at which the selection gradient is zero. Horizontal (red) arrows indicate that the selection gradient is

positive below the fitness map, and negative above. The filled circle indicates the eco-evolutionary equilibrium arising in this graphical example.

4We use the word ‘predator,’ rather than the more common word, ‘grazer’,to refer to organisms that consume microalgae, because the microalga is nec-essarily killed when it is eaten. We note that organisms that consumemicroalgae have historically been called ‘grazers’, perhaps because their preyis photosynthetic, or perhaps because the distinction between entire organ-

isms and ‘parts’ of organisms is less clear in planktonic autotrophic communi-ties (which include colonies, filaments and aggregates) than their terrestrialcounterparts. Given our focus on commonalities and contrasts between aqua-tic and terrestrial communities, we opt for semantic consistency.


Review and Synthesis Private/public goods in eco-evolutionary dynamics 83


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(Teegarden et al. 2001; Vanderploeg et al. 2001). Indeed,

introduced (Schoenberg & Carlson 1984) and native (Wang

et al. 2010) selective predators can promote the growth of

toxic cyanobacteria in natural communities, underscoring the

potential for the indirect effects of selective predation to

facilitate TABs.

In Fig. 2a, the fitness map intercepts the ecology map on its lower stable branch, thus predicting a stable eco-evolutionary

equilibrium of low density and intermediate toxicity. Figure 2b – d illustrates the destabilisation, and potential re-stabilisation of

the original eco-evolutionary equilibrium as caused by the emergence of a public good. This may happen through shifts in the

ecology map (Fig. 2b), the fitness map (Fig. 2c), or both (Fig. 2d), thus relocating the fitness map in between the two stable

branches of the ecology map. Following destabilisation, higher toxicity evolves (‘private good’ of Step 1 in the emergent public

goods sequence) whilst the population density increases modestly, thus remaining in the ‘low density’ state. At some critical

threshold of toxicity, the low-density equilibrium becomes unstable and the system shifts to its alternate ecological stable state

(high density; ‘positive feedback’ of Step 2). At high density, there is now selection against toxicity (‘public good’ of Step 3),which leads eventually to the collapse of the population on to its original (low density) ecological state, with reduced toxicity

(‘tragedy of the commons’ of Step 4). A similar type of eco-evolutionary hysteretic cycle was first described by Dercole et al.

(2002) in a different biological context (evolution of body size in a competitive system).

Figure 2 emphasises that each of these shifts may be caused by some environmental perturbation. In Figure 2b, the environ-

mental perturbation moves the ecology map upward; this might be the result of some nutrient input, which would cause an

increase in density independently of the trait value, or circulation patterns that cause the formation of dense cell aggregations.

In Figure 2c, the environmental perturbation moves the fitness map upward, as a consequence of selection becoming more

favourable to toxicity at low density. This might be caused by increased densities of prey, such as soft-bodied algae. This change

causes higher competition for inorganic nutrients, but simultaneously results in greater availability of organic nutrients derived

from intraguild predation. Both changes favour increased reliance on toxin-mediated predation. Because shifts in the ecology

and/or fitness maps may not be permanent, the system is predicted to return to its original eco-evolutionary equilibrium as the

effects of the environmental perturbation dissipate. This might occur at various points along the cycle, thus potentially generat-

ing a rich array of bloom dynamics, varying notably in their duration and toxicity at the onset of the termination phase.Finally, Figure 2e and f underscore that the existence of alternate stable ecological states is not strictly required. In Figure 2f,

both the ecology and fitness maps are destabilised, causing the replacement of the original eco-evolutionary equilibrium with a

stable limit cycle. Steps 1 – 4, however, still apply to the four different phases of the cycle (increase in toxicity, increase in

density, decrease in toxicity and decrease in density).

Box 1 Continued

Mean trait value

(a)

(b)

(e)

(f)(c) (d)

Response to environmental fluctuation

E c o l o g i c a l s t a

t e

( e .

g .

p o p u l a t i o n

s i z e )

Figure 2 Alternative eco-evolutionary scenarios yielding emergent public goods. Open circles indicate the location of eco-evolutionary equilibria prior to

environmental perturbation, and dotted curves indicate instability (ecological instability along the ecology map, or divergent selection around the fitnessmap). In (a – d), the ecology map is S shaped, with alternate ecological equilibria over a range of trait values. In (a), prior to environmental

perturbation, the eco-evolutionary equilibrium is on the lower (i.e. ‘low density’) branch. In (b – d), some environmental perturbation shifts the ecology

map (b), the fitness map (c), or both (d). As a result, there is positive (negative) selection on the trait at low (high) density, triggering a wide eco-

evolutionary oscillation (grey arrows). In (e – f), there are no alternative ecological equilibria in the ecology map. Instead, instability in both ecology and

fitness maps (f) can cause stable eco-evolutionary limit cycles when ecological and evolutionary change occur over similar timescales.




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Toxicity as venom: incapacitating and killing prey

Many (if not most) TAB-forming eukaryotic microalgae are

mixotrophs, and may acquire limiting nutrients by engulfing

particulate organic material, including bacteria, detritus and

living (or recently killed) cells (Burkholder et al. 2008). Toxi-

genesis is frequently upregulated in response to nutrient stress,

consistent with a role in predation. This diverse group mainly

comprises the dinoflagellates, haptophytes and raphidophytes.

Toxicity in these species was long believed to result from

secretion of extracellular toxins into the water column;

however, a series of studies using permeable membranes or

other methods to separate live toxic cells from targets has

shown that toxicity of intact cells is significantly increased by

(or entirely dependent upon) physical contact with targets

This basic finding has been reported for many important

TAB-forming mixotrophs (Table 2). The negative effects

of these lineages on heterospecifics thus result from direct

cell – cell interactions, rather than action at a distance via

secreted exotoxins.

Direct microscopic observations of predator – prey interac-

tions provide compelling evidence for the offensive utility of

toxins at the cell-level. The ‘red tide’ dinoflagellate

Karlodinium veneficum secretes toxins that incapacitate motile

Box 2 Emergent public goods and established models of cooperation.

Semantic confusion and discipline-specific terminology are major barriers to interdisciplinary work. Such problems arise, in

part, due to the tendency to propose new terminology for existing concepts. Thus, it is worthwhile to consider the similarities

and differences between the framework we have advanced here and closely related models in evolutionary game theory.

The Public Goods Game (PGG).

Together with its two-player equivalent, the Prisoner’s Dilemma, the PGG has been enormously influential in biology (Doe-

beli & Hauert 2005). In the PGG, players are given an endowment, and may choose whether to ‘invest’ in the public good (co-

operate), or keep the endowment for themselves (defect). The total investment of all players then appreciates, and is distributed

evenly to all players. The game highlights the potential for conflict between individual self-interest and the good of the group:

individuals may always improve their net reward by defecting, regardless of the behaviour of the other players; however, the

group is best served by all players investing. Defection is the only evolutionarily stable strategy in the absence of additional

mechanisms to foster cooperation (e.g. reputation, iterated games, policing).

The Snowdrift Game (SG)

The SG has historically been less studied (Doebeli & Hauert 2005), but may present a more realistic alternative to the PGG

for many biological situations (Gore et al. 2009). As in the PGG, the highest payoff in the SG goes to a defector interacting

with a (high frequency of) cooperator(s). However, defectors playing with other defectors actually do worse than would a coop-

erator in the same situation. Thus, given that a partner will cooperate, the best option is to defect; given that a partner will

defect, the best option is to cooperate. This game corresponds to situations in which the consequences of defection are especially

dire – for example when survival depends on some level of cooperation. Translated into an evolutionary context, the SG payoff

matrix leads to negative frequency-dependent selection for cooperation, which leads to coexistence between cooperators and

defectors.

In some ways, the emergent public goods scenario would seem more similar to the SG. In fact, the former converges on the

latter in the special case of internally driven transitions between private and public goods, as illustrated in the maintenance of

invertase production in yeast (see ‘Ecologically driven switches between private and public goods in laboratory microbes’). In

this situation, the turnover of the ‘public good’ (accessible sugars) due to secretion and uptake is presumably fast relative to

population dynamics. As a result, the emergence and collapse of the public good quickly and smoothly tracks the population

state (Sanchez & Gore 2013). Thus, although selection reversals are not driven directly by frequency, the tight coupling between

the frequency of producers, environmental state, and selection for production make the SG an excellent approximation.

However, in many cases (including TABs), the emergence and collapse of public goods may occur over longer time scales

and/or involve large-scale, discrete switches between ecological states. In these situations, the SG game is not a good fit. For

example colonial microalgae may indirectly benefit unicellular competitors via negative impacts on shared predators, whereas

the success of unicells is limited by positive effects on the same predator (Becks et al. 2010). However, these effects are mediated

by the population dynamics of the predator, which are slower than those of the microalgae. As a result, there is a lag between

changes in the states of the population (frequency of colonies) and the public good (reduced predation). This leads to dramatic,

large-scale switches between high- and low-predation environments, within which colony formation behaves like a private or

public good respectively. As explained conceptually in Box 1, these switches may occur between alternate ecological stable states

(Fig. 2a – d), or as rapid phases along an eco-evolutionary cycle (Fig. 2e – f).

The possibility for true public goods traits to emerge from changes to ecological context, rather than evolving due to selection

for cooperation, provides an alternative historical explanation for the existence of a public goods trait. Although the rapid

acceptance of social evolutionary principles in microbial ecology has undoubtedly stimulated a great deal of exciting and cre-

ative research, the dominance of any single framework can become pathological, particularly when it obscures simpler alterna-

tive explanations (Rainey et al. 2014). The perceived conflict between genetic and ecological explanations of cooperation are

likely to persist in the absence of frameworks capable of exploring the relationships between evolutionary and ecological aspects

of transitions in sociality.




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prey prior to ingestion (Sheng et al. 2010). Another dinoflag-

ellate, Alexandrium pseudogonyaulax, secretes extracellular

‘toxic mucous traps’ that facilitate predation by snaring motile

prey (Blossom et al. 2012). The haptophyte Prymnesium par-

vum kills prey following a relatively brief period of direct con-

tact, and then engulfs the lysed material (Driscoll et al., in

prep). Finally, cells of two raphidophytes excrete toxic

mucous bodies, which remain bound to the cell surface (Ya-

masaki et al. 2009) and snare small, live prey prior to inges-

tion (Jeong 2011).

Toxin-mediated predation suggests a plausible ‘private’

benefit of toxin production, even when toxic cells are rare. Just

as predators of chemically defended microalgae vary in their

selectivity, the degree to which offensive toxicity is ‘incentivized’

at the cell-level will depend on the abundance of suitable prey.

Toxic mixotrophs vary widely in their prey specificity, and may

be limited by the size (Hansen & Calado 1999) or physical

defences of prey, even when prey may be killed. The rigid, silic-

eous frustule of diatoms in particular appears to prevent phago-

cytosis by the otherwise omnivorous dinoflagellate Karlodinium

armiger (Berge et al. 2008) and haptophyte P. parvum (Till-

mann 1998; Driscoll et al. 2013). However, in sufficient densi-

ties, both of these species employ collective ‘wolf pack’

strategies of predation upon larger organisms, including ani-

mals (Berge et al. 2012; Remmel & Hambright 2012).

From cell- to community-level effects

Toxic algae blooms have long been viewed as the outcome

of population-scale adaptive strategies, requiring the con-

certed efforts of billions of cells. According to this view

the primary ecological benefits responsible for the evolution

of toxigenesis are the cooperative elimination of competitors

(allelopathy) and predators (‘grazer killing’). Objections to

the tendency to view toxicity as cooperation have been

raised fairly regularly over the past three decades (e.g

Lewis 1986; Thornton 2002; Jonsson et al. 2009). In fact, if

cell- or colony-level selection is sufficient to favour toxicity

through direct trophic interactions, many of the most con-

spicuous ecological benefits associated with blooms are

byproducts from an evolutionary standpoint. For example

toxins that deter selective predators (Teegarden 1999;

Guisande et al. 2002) may, in sufficient densities, kil

(Barreiro et al. 2006) or impair (Teegarden et al. 2008)

predators that do not discriminate among toxic and non-

toxic prey. Similarly, lytic chemicals that facilitate intraguild

predation can kill even those competitors which may not be

consumed (Driscoll et al. 2013) or suppress predators of the

toxic population (Adolf et al. 2007; Waggett et al. 2008).

Thus, multiple novel ecological benefits may emerge beyond

threshold cell concentrations of toxic cells (Fig. 3), poten

tially leading to positive feedbacks between density and ne

growth (Irigoien et al. 2005; Sunda et al. 2006).

The transition from relatively subtle, cell-level ‘private’ func-

tions of toxicity to conspicuous, community-scale ‘public good

benefits frequently depends on threshold densities of toxic

cells. The dinoflagellate Karlodinium armiger and haptophyte

Prymnesium parvum can be safely consumed by animal and

microbial predators at low densities; however, beyond thresh-

old concentrations, the trophic interaction reverses, and the

Table 1 Studies that have demonstrated cell- or colony-level advantages of toxicity

Toxic alga Predator References

Defence Cyanobacteria Microcystis sp. Native zooplankton Wang et al. (2010)

Mollusc Dreissena polymorpha Vanderploeg et al. (2001);Raikow et al. (2004)

Cladoceran Bosmina longirostris Schoenberg & Carlson (1984)

Nodularia spumigena Copepods Various Gorokhova & Engstrom-Ost (2009)

Dinoflagellate Alexandrium fundyense Arthropod Acartia hudsonica Colin & Dam (2003)

Alexandrium sp. Copepods Three species Teegarden (1999)Alexandrium minutum Copepod Acartia tonsa Selander et al. (2006)

Karenia mikimotoi Copepods Two species Schultz & Kiørboe (2009)

Haptophyte Emiliania huxleyi Mic rob ial p red ators Va riou s Str om & Br ight (20 09)

Heterokontaphyte Heterosigma akashiwo Various Graham & Strom (2010)

Toxic alga Prey Reference

Offence Dinoflagellate Alexandrium pseudogonyaulax Various microalgae Blossom et al. (2012)

Karlodinium veneficum Microalga Storeatula major Sheng et al. (2010)

Haptophyte Prymnesium parvum Microalga Dunaliella tertiolecta Driscoll et al. (2013)

Heterokontaphyte Heterosigma akashiwo Cyanobacteria Synechococcus Jeong (2011)

Chattonella ovata

References are available in Supplemental Materials.

Table 2 Evidence that direct cell contact is required for toxicity

Toxic alga Method References

Dinoflagellate Pfiesteria Membrane Vogelbein et al. (2002)

Heterocapsa Filtrate Uchida et al. (1995);

Yamasaki et al. (2011)

Karenia Me mb rane Zo u et al. (2010)

Cochlodinium Membrane Yamasaki et al. (2007)

Karlodinium Filtrate Berge et al. (2012)

Haptophyte Prymnesium Membrane;

filtrate

Remmel & Hambright

(2012)





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microalgae kill and feed upon their predators (Tillmann 2003;

Berge et al. 2012). Although these direct interactions may ben-

efit the individual cells involved, there are nevertheless broader

beneficial impacts not only for conspecifics, but for all (resis-

tant) potential prey of the killed predators. A similar transition

may occur simply via changes in abundances of different

predators. For example individual colonies of toxic cyanobac-

teria benefit through toxin production when predators are cap-

able of avoiding or rejecting toxic colonies (Table 1); however,

their negative effects on indiscriminate predators following

ingestion can only benefit all remaining potential prey, includ-

ing non-toxic populations (Table 2; Figure 1c).

Dense, highly toxic populations may also harm

heterospecific populations that (directly or indirectly) benefit

toxic lineages. Susceptible prey populations provide direc

benefits to individual toxic predators, but are unlikely to

persist at appreciable densities during ecosystem-disruptive

blooms of their predators (Adolf et al. 2008). Similarly

even highly selective predators may suffer at extreme toxic

population frequencies or densities (Vanderploeg et al.

2009). Loss of susceptible prey and selective predators

would remove agents of selection favoring toxin production

at the cell-level for offensive and defensive functions, respec-

tively.

(a)

(b)

(c)

Figure 3 Examples of transitions from private advantages to public goods. (a) Toxins evolved to immobilise and kill prey may poison predators when toxic

cells are sufficiently abundant. (b) Toxins that assist in predation may also act as allelochemicals when they target non-prey competitors. (c) Toxins that

defend individual cells or colonies by dissuading selective predators may impair or kill indiscriminate predators at sufficient densities.




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Abiotic processes have long been seen as playing major

roles in the initiation and termination of most TABs. In many

specific locations, the presence or absence of a TAB in any

particular season may depend entirely upon well-understood

climatic or physical factors. For example, blooms may occur

when wind shears drive surface circulation patterns that con-

centrate normally sparse toxic cells in relatively small volumes

of water in coastal areas (Tester & Steidinger 1997), or when

droughts increase the nutrient levels in lakes fed by runoff

from agricultural lands (Paerl & Huisman 2009). The occur-

rence of TABs depends on the emergent benefits of collective

toxicity in populations that exceed threshold concentrations,

by whatever mechanism (e.g. selective grazing and prolifera-

tion in cyanobacteria, spatial aggregation in dinoflagellates).

In general, whereas the possibility of toxicity serving as an

emergent public good depends on features of the toxic popu-

lations and their ecological communities, the realisation of this

possibility in any one time or place will depend on a number

of (abiotic and biotic) environmental factors.

Genetic and toxicity diversity of bloom populations

The idea that bloom populations may undergo significant

evolutionary change over the course of a TAB has gained

increasing attention lately. Individual toxic blooms were long

assumed to comprise a single, dominant clone (Thornton

2002), and populations that lack heritable variation simply

cannot evolve. However, evidence for intra-population genetic

diversity of a few TAB-forming species has been accumulating

since before the 1990s (Table 3), a trend that has intensified in

recent years as sequencing technologies become more practical

and affordable. At present, substantial genetic diversity has

been documented within blooms formed by most of the main

toxic taxa (Table 3).

Bloom populations may harbor considerable diversity in

heritable functional traits, including toxic potential. The

molecular basis of variation in key toxins (e.g. microcystin) is

relatively well understood in the cyanobacteria, permitting

researchers to use culture-free environmental sequencing

methods to track frequencies of toxic and non-toxic

genotypes. As a result, variation in the toxic potential of

cyanobacterial populations has been measured with unparal-

leled resolution through time in different species and environ-

ments (Table 4).

The situation is substantially more complicated in the TAB-

forming eukaryotes: in the absence of knowledge of the

molecular mechanisms underlying toxin production, assessing

heritable variation in toxic potential requires isolation, cultur-

ing and characterisation of multiple strains. Nevertheless

several studies have reported heritable variation in toxicity

among co-occurring isolates within eukaryotic TAB popula-

tions (Table 4). In fact, even very closely related, co-occurring

genotypes may differ substantially in toxicity and growth rate,

suggesting that substantial functional variation may exist even

in relatively genetically similar populations (Loret et al. 2002).

In some cases, other important traits appear to co-vary with

toxicity across relatively few isolates, including behaviours

related to predation (Bachvaroff et al. 2009; Driscoll et al.

2013) and colony-formation in the cyanobacteria (Kurmayer

et al. 2003). However, deeper sampling and/or an improved

understanding of the genetic and physiological mechanisms

underpinning toxicity variation will be required to determine

whether and to what extent such traits are co-regulated or

functionally integrated with toxigenesis.

The relatively few studies that have managed to track

genetic or phenotypic changes in bloom populations suggest

the potential for rapid evolution over the lifetime of a single

bloom. Toxic cyanobacteria show high variation in toxicity

across space (Wilson et al. 2005) and over the course of a

single bloom (Briand et al. 2009). However, the evolutionary

dynamics of toxicity within blooms may diverge in differen

environments, as well as in the same environment over

Table 3 Evidence for genetic and toxicity variation within toxic blooms formed by various taxa

Toxic alga

Toxicity

variation?

Variation

in time? References

Cyanobacteria Planktothrix agardii Yes Yes Welker et al. (2004); Briand et al. (2008)

Microcystis aeruginosa Yes Yes Wilson et al. (2005); Briand et al. (2009)

Alexandrium catenella Yes n.d. Aguilera-Belmonte et al. (2011)

Alexandrium ostenfeldii n.d. n.d. Gribble et al. (2005)

Alexandrium fundyense n.d. Yes Erdner et al. (2011); Richlen et al. (2012)

Cochlodinium polykrikoides n.d. n.d. Park et al. (2014)

Karenia brevis Yes n.d. Loret et al. (2002)

Alexandrium tamarense Yes n.d. Tillmann et al. (2009); Alpermann et al. (2010)

Gambierdiscus sp. Yes n.d. Nishimura et al. (2013)

Dinoflagellate Karlodinium veneficum Yes n.d. Bachvaroff et al. 2009; Calbet et al. (2011)

Prymnesium parvum n.d. n.d. Barreto et al. (2011)

Yes n.d. Driscoll et al. (2013)

Haptophyte Emiliania huxleyi n.d. n.d. Iglesias-Rodriguez et al. (2006)

Heterosigma akashiwo Yes* n.d. Fredrickson et al. (2011)

Heterokontaphyte Pseudo-nitzchia cuspidata Yes† n.d. Lundholm et al. (2012)

Pseudo-nitzchia sp. Yes† n.d. Thessen et al. (2009)

*Only one strain isolated at a time; a nontoxic strain was isolated at the end of the bloom.

†We have largely ignored domoic acid, due to uncertainty regarding its eco-physiological function.





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subsequent years (Briand et al. 2005). The variation in the

eco-evolutionary patterns of these populations is in some ways

unsurprising, considering the many potential direct and

indirect effects of toxigenesis in this group, as well as the

potential for coevolution with important predators (see ‘Co-

evolution and the fate of blooms’ below). Blooms formed by

Alexandrium fundyense in a closed off salt marsh were highly

divergent from an adjacent coastal bloom, and showed extre-

mely fast genetic turnover (populations differentiated in as

little as 7 days) (Richlen et al. 2012). Rapid adaptation is

again a likely explanation, but information about pheno-

typic change will naturally be required to identify agents of

selection.

Is the tragedy of the commons relevant to TABs?

The final ‘stage’ in the emergence of a public good is the ‘tra-

gedy of the commons’ (Hardin 1968), in which exploitation of

the benefits of toxicity by non-producers results in the deterio-

ration of the public good. This intriguing possibility is

relatively unexplored in the TAB literature, at least as it

pertains to intraspecific variation in toxigenesis. We explore

the possibility of ‘cheating’ with respect to the two basic

large-scale public goods that may emerge from the success of

toxic lineages: impairment/killing of predators, and allelopa-

thy. In both cases, substantially more work has focused on

interspecific effects, probably due to technical challenges with

tracking the dynamics of genotypes (compared with distinct

species) or a tendency to view toxic populations as function-

ally homogeneous (Burkholder & Glibert 2006). Nevertheless,

exploitation of emergent public goods by heterospecifics

reflects a conceptually similar ecological (rather than evolu-

tionary) path to the tragedy of the commons.

Researchers have long recognised the important roles of

non-toxic prey for the feeding behaviour and health of preda-

tors exposed to toxic prey. Non-toxic prey may have two

contrasting (but not necessarily mutually exclusive) impacts

on predators, which ultimately impact the toxic population in

opposite ways. Selective predators may target non-toxic prey

when available, but consume toxic prey in the absence of non-

toxic alternatives. Alternatively, non-toxic algae may have a

positive effect on the health of indiscriminate predators, which

consume both toxic and non-toxic prey. Selective predators

are frequently observed in TABs (and may actually contribute

to their formation and persistence), whereas indiscriminate,

high-throughput feeders like Daphnia may be capable of con-

trolling relatively sparse toxic populations precisely because

they (typically) do not avoid toxic lineages (Schoenberg &

Carlson 1984; Gobler et al. 2007). Thus, if non-toxic prey is

able to increase to sufficient densities within a TAB, they may

compromise the ‘public good’ of protection from indiscrimi

nate predators and even facilitate the re-emergence of these

important populations (Schoenberg & Carlson 1984)

Although laboratory experiments have demonstrated this

effect to various degrees and over limited scales, we are

unaware of field studies that have deliberately manipulated

the relative abundances of toxic and non-toxic prey.

Even less is known about the potential for non-toxic

resistant populations to undermine the competitive advan-

tage conferred by allelopathy. Because allelopathy necessar-

ily requires that toxins have broad-spectrum impacts on co-

occurring microalgae, this particular benefit is most likely to

assist producers of ‘offensive’ toxins. (However, we note

that lytic toxins produced by predatory algae may neverthe-

less be harmful to predators of these species (John et al.

2002, 2014)). In at least two cases, ‘non-toxic’ lineages iso-

lated from TABs formed by predatory taxa showed distinct

preference for autotrophic growth (Bachvaroff et al. 2009;

Driscoll et al. 2013); however, TAB-forming mixotrophs are

typically poor competitors for inorganic nutrients (Bur-

kholder et al. 2008). It is possible that a preference for

autotrophic growth (and corresponding reduction in toxicity)

following reductions in prey populations and extinction of

most autotrophic competitors represents a short-term (and

short-sighted) adaptation to TAB conditions. Although one

study found limited evidence that a non-toxic subpopulation

undermined allelopathy as an emergent public good (Dris-

coll et al. 2013), more work is needed to test this prediction

in this and other taxa.

Interestingly, many TABs formed by allelopathic species

harbor significant populations of heterospecific microalgae

(Michaloudi et al. 2009; Hakanen et al. 2014; Poulson-

Ellestad et al. 2014), and co-culture tests have found that

co-occurring heterospecifics may be resistant to TAB-forming

populations (Hakanen et al. 2014; Poulson-Ellestad et al.

2014). Such non-toxic, resistant populations have the potential

to compete directly with allelopaths, partially nullifying this

emergent benefit (Chao & Levin 1981; Durrett & Levin 1997).

Furthermore, if these lineages reduce the allelopathic potential

of the population, it is possible that they might compromise

Table 4 Evidence for ‘public good’ benefits of toxicity extending to non-toxic conspecifics or heterospecifics

Toxic microalga Target Benefit Non-toxic beneficiary

Public good

undermined? References

Cyanobacteria Microcystis aeruginosa Tilapia P Conspecific Yes Keshavanath et al. (1994)

Cladoceran P Conspecific Yes Van Gremberghe et al. (2009)

Dinoflagellate Alexandrium fundyense Microbe P Conspecific No John et al. (2014)

Alexandrium minutum Copepod P Conspecific Yes Barreiro et al. (2006)

Alexandrium sp. Native copepod species (4) P Heterospecific n.d. Teegarden et al. (2008)Karlodinium veneficum Microbe P Conspecific Yes Adolf et al. (2007)

Copepod P Conspecific Yes Waggett et al. (2008)

Haptophyte Prymnesium parvum Co-occurring centric diatom C Conspecific Yes Driscoll et al. (2013)

‘P’ is ‘reduced predation pressure’; ‘C’ is ‘reduced competition’. References are available in Supplemental Materials.




10/17

the low-competition ‘public good’ established by their toxic

competitors and provide a window of opportunity for suscep-

tible populations to become re-established. These observations

underscore the ecological (as well as evolutionary) instability

of emergent public goods within diverse, unstructured

communities (Fig. 4).

Abiotic processes are well known to play central roles in

the initiation, persistence, and termination of TABs, often by

magnifying or ameliorating the ecological effects of toxigenic

populations. For example eutrophication permits explosive

growth of autotrophs, but selective predators are likely

responsible for the rise of toxic lineages in particular

(Schoenberg & Carlson 1984; Gobler et al. 2007; Wang et al.

2010). Hydraulic processes can trigger or disrupt blooms by

concentrating or diluting toxic populations (Schwierzke-Wade

et al., 2010), respectively, thus quickly moving the population

above or below key thresholds for novel ecological benefits

(e.g. reduced predation and competition). The accumulation

of non-toxic conspecifics may work in concert with well-

recognised mechanisms (e.g. hydraulic flushing, nutrient

depletion) to facilitate the re-establishment of important, sus-

ceptible populations. This possibility remains almost entirely

unexplored, and has the potential to inform novel, environ-

mentally benign bloom remediation strategies.

SYNTHESIS: WHAT CAN TOXIC ALGAL BLOOMS

TEACH US ABOUT ECO-EVOLUTIONARY FEEDBACKS

IN NATURE?

Toxic blooms result from a positive feedback between cell

density and population growth. Together with individual-level

selection for toxicity at low cell density, environmental factors

that cause local increases in density (e.g. aggregation due to

currents; eutrophication) may be required to drive the popula-tion across a threshold of total toxicity. Novel ecological

effects of toxins then accumulate as densities rise, including

the destruction or suppression of natural enemies within the

plankton community. The dieback of key susceptible popula-

tions (or the rise of resistant lineages), particularly potentia

prey and predators of the toxic population, may relax cell-

level selection for toxicity. The concurrent accumulation of

widely distributed benefits of toxigenesis and removal of

agents of selection for toxicity operating at the cell-level may

then result in the emergence of a massive public goods game.

The basic elements of this hypothesis are intended to be

quite general and may, in principle, be applied to both aquatic

and terrestrial ecosystems. Indeed, TABs are formed by a

deeply divergent group of prokaryotes and eukaryotes, despite

the many profound differences in toxins and eco-physiology

(a)

(d)

(c)

(b)

Figure 4 Schematic representation of eco-evolutionary feedback during a TAB. (a) Under non-bloom conditions, toxin production is favoured by selection

at the cell-level (private good). (b) Localised increases in toxic cell density, through growth, aggregation or physical concentration, trigger the emergence of

large-scale ecological advantages, which re-structure the community (positive feedback). (c) In the absence of cell-level agents of selection that favour toxin

production, non-toxic, resistant lineages (potentially including conspecific and heterospecific lineages) invade the bloom (public good). (d) Bloom

termination may be triggered by a variety of factors, including exogenous (e.g. changes in temperature), endogenous (e.g. decreased toxicity; tragedy of the

commons), or complex interactions of many factors (e.g. hydraulic flushing and diminished toxicity permit re-establishment of susceptible community).




11/17

that separate these species. Propensity to form TABs may

therefore result from different toxin-mediated ecological

‘strategies’ (including ‘defensive’ and ‘offensive’) employed by

evolutionarily distant taxa. Might the patterns and processes

that underlie TAB formation transcend the aquatic/terrestrial

divide?

Emergent public goods in terrestrial and laboratory systems

Evidence from a variety of natural and laboratory systems

suggests that many important traits may vary (continuously

or more discretely) between exclusively benefiting the individu-

als that express them and helping a broader set of beneficia-

ries. Whether a trait represents an investment in the ‘private’

or ‘public good’ may be determined by the frequency or

density of bearers, the physical environment, interactions with

other members of the community, or various combinations of

these factors. Although the notion of public goods is most

frequently associated with conspicuous extra-organismal ‘in-

vestments’ (e.g. secreted products, constructed habitats), it is

actually the spatial extent of the beneficial effects of a trait

that defines its position along the private-to-public continuum.

Below, we briefly summarise well-studied illustrations of key

aspects of emergent public goods from terrestrial plant

communities, animal predator – prey interactions and labora-

tory microbial communities, before returning to the question

of TABs as model systems for the broader study of eco-

evolutionary feedbacks.

Terrestrial plant communities: public goods arise from indirect

interactions

Ecologists have long recognised the potential for plants to

influence one another indirectly via their direct interactions

with animals, fungi, and microbes, which may ‘spill over’ to

impact neighbours. The specific effect on neighbours naturally

depends on the nature of the interaction: a palatable neigh-

bour may be helpful or harmful, depending on whether it

attracts herbivores over small (inter-individual) or large (inter-

patch) scales; the inverse is true of unpalatable neighbours.

Thus, a palatable species may benefit from reduced grazing

pressures in the presence of a heterospecific that invests heav-

ily in defence chemicals, if grazers select among ‘patches’

rather than individual plants (Ruttan & Lortie 2015). Similar

potentials exist for neighbour-mediated effects when volatile

compounds signal herbivore attack (Dolch & Tscharntke

2000) or summon carnivorous ‘bodyguards’ that benefit plants

by attacking herbivores (Dicke & Baldwin 2010).

Costly traits involved in influencing interspecific interactions

may benefit neighbouring conspecifics, which may or may not

invest in these same traits. This possibility has been studied in

the context of defences against herbivores, as well as the

production of competitive compounds that harm interspecific

competitors. Two examples of such indirect intraspecific inter-

actions involve polymorphisms in conspicuous defences

against insect herbivores: the bent ‘candy cane’ stem of the

tall goldenrod (Solidago altissima; (Wise 2009)), and the pro-

duction of trichomes resulting in a ‘hairy’ phenotype in Ara-

bidopsis halleri (Sato et al. 2014; Sato & Kudoh 2015). In

both cases, the defensive phenotype conferred herbivore resis-

tance for rare plants in the presence of high proportions of

undefended plants, consistent with a private good. However

defended plants gained additional benefits at a ‘patch’ leve

when surrounded by high frequencies of other defended

plants. Furthermore, both studies found evidence that unde-

fended plants may enjoy reduced herbivory in patches domi-

nated by defended plants (although not to the same extent as

defended individuals), consistent with defence as a partially

privatised public good (Wise 2009; Sato et al. 2014).

The spatial scales over which the benefits of plant defences

accrue depend on the dominant herbivore(s), which may vary

dramatically in selectivity, motility, generation time, and toler

ance. Most evidence that the benefits of chemical defences can

extend to undefended heterospecific neighbours has come

from studies that focus on large mammalian herbivores (see

Ruttan & Lortie 2015 and references therein). In contrast

insect herbivores are generally expected to be more selective

over local scales, shifting the scale of benefits towards the

individual-level (Ruttan & Lortie 2015), consistent with a

private good. In fact, the ‘patch-level’ benefits of trichomes

depends on the specific insect herbivore: although a flightless

beetle and butterfly both preferentially grazed undefended

plants, the patch-level benefits of defence were only observed

in the slow-moving flightless beetle (Sato & Kudoh 2015)

Thus, the balance between private and public benefits of

defensive adaptations may shift with the abundance and

activity of functionally distinct herbivores, as well as loca

abundance of defended plants. Based on the relatively few

empirical studies that have addressed these issues, it appears

that (1) defended plants can gain a relative fitness advantage

when rare, or when selective herbivores dominate; (2) high fre-

quencies of defended plants may benefit all plants within a

‘patch’ (although this pattern depends on herbivores), and (3)

undefended plants may benefit from growth near high densi-

ties of defended conspecifics. Whether and to what extent (4)

regional abundances of different herbivores can be driven by

frequencies of defended plants remains, to our knowledge,

unknown.

Many plants employ secreted toxins that suppress

heterospecific competitors (allelopathy). Different genotypes

of the black mustard (Brassica nigra) invest to different

degrees in sinigrin production, which (among other effects)

inhibits heterospecific competitors without impacting con-

specifics (Lankau 2008). High sinigrin producers out-perform

a low-producing lineage during invasion of established

heterospecific communities and were more resistant to inva-

sion by heterospecifics; however, low-producers excelled in

intraspecific competition (Lankau & Strauss 2007). Indeed,

the sign of selection on sinigrin content reversed between com-

munities in which B. nigra was rare or common, favouring

reduced sinigrin levels as B. nigra densities increase (Lankau

& Strauss 2007). Finally, allelochemicals are partly responsible

for the success of the invasive plant Alliaria petiolata within

native communities in North America; however, the competi-

tive ability of these populations deteriorates over time due to

selection for reduced allelochemical production (Lankau et al.

2009). Thus, (1) allelochemical production yields advantages

to individual plants when invading communities dominated by




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susceptible heterospecifics, (2) high patch-level allelochemical

production suppresses heterospecific invaders, (3) selection

favours reduced investment in allelochemicals when con-

specifics are common (and heterospecifics rare), and (4) popu-

lation-level competitive ability is undermined by decreasing

investment in allelochemicals.

Individual- and group-level advantages of chemical defences inanimals

Many insects have evolved defensive endotoxins that discour-

age predation. However, this mode of defence requires that

the predator taste the prey, which frequently results in injury

or death to the prey before the predator can change its

behaviour. As a result, defensive toxins are frequently

accompanied by visual warning signals, which allow experi-

enced predators to avoid toxic prey altogether. In this scenar-

io, a few toxic animals benefit conspecifics by ‘teaching’

predators to avoid similar individuals. However, non-toxic

prey may evolve to mimic these signals, potentially compro-

mising the reliability of the signal in the eyes of the predator.

The potential private (individual-level) and public (group-

level) advantages of chemical defences have been investigated

experimentally using birds as model predators. Skelhorn &

Rowe (2007) found that non-defended prey models were

preferentially consumed as they became more common rela-

tive to defended prey, whereas Jones et al. (2013) found that

rising local frequencies of non-toxic mimics resulted in higher

predation rates for all targets, regardless of defence. A recent

experiment by Speed et al. (in prep) neatly captured both pri-

vate and public benefits of defence: survival following initial

attacks is largely dictated by individual-level defensive status,

whereas initial attack rates decrease for all prey when

defended insects are locally common. Thus, (1) defence may

improve individual-level survival regardless of neighbour

strategies, (2) local attack frequencies decline with increased

proportions of defended prey, (3) undefended prey experience

reduced attack rates in otherwise well-defended groups, and

(4) rising frequencies of undefended prey may (or may not)

increase local attack frequencies for all phenotypes.

Ecologically driven switches between private and public goods in

laboratory microbes

The past decade has seen a rapid increase in the attention

paid to microbial social behaviours, particularly those medi-

ated by secreted metabolites. The term ‘public good’ is fre-

quently used to refer to these beneficial, extracellular

products, based on the assumption that individual producers

cannot ‘privatise’ the positive effects of extracellular products

(K€ummerli & Ross-Gillespie 2013). However, there is

mounting evidence that secreted products may yield relative

fitness advantages to producing bacteria in the presence of

non-producing lineages, consistent with a private good (Zhang

& Rainey 2013; Scholz & Greenberg 2015).

Some strains of brewer’s yeast (Saccharomyces cerevisiae)

secrete invertase, an enzyme that digests sucrose into glucose

and fructose, which may then be taken up by cells. However,

some strains do not produce invertase, and are able to benefit

from invertase produced by others (Greig & Travisano 2004).

Non-producers can gain a relative fitness advantage when

grown with high densities of producers in structured (Greig &

Travisano 2004) and unstructured (Gore et al. 2009) environ-

ments. However, producers enjoy direct fitness advantages in

sparse populations (Greig & Travisano 2004; Gore et al. 2009).

Thus, the degree to which benefits of production are localised

to producer cells is determined by their density; however, densi-

ties can drop as non-producers accumulate, consistent with a

‘tragedy of the commons’ (Sanchez & Gore 2013). Together,

these results show that (1) individual producers ‘privatise’ the

benefits of production in sparse populations; (2) population

density increases with the proportion of producers; and (3)

non-producers exploit invertase produced by others in dense

populations, ultimately (4) undermining the ‘public good’ and

causing population declines. These ingredients yield a full eco-

evolutionary feedback that closely approximates the snowdrift

game, which allows stable coexistence between producers and

non-producers (Sanchez & Gore 2013; Box 2).

The formation of multicellular aggregates or colonies is a gen-

eral defence against predation by relatively small, gape-limited

predators, and is common among microbial taxa. In the unicel-

lular green alga, Chlamydomonas reinhardtii , predation by the

small rotifer Brachionus calyciflorus resulted in the rapid

appearance of palmelloids [small, matrix-encased colonies

(Becks et al. 2010)]. Palmelloid production was heritable (i.e

not inducible, as is the case in many microalgae), and resulted

in resistance to grazing at a cost of reduced intraspecific com-

petitive ability. In mixed cultures, rotifers preferentially con-

sumed unicells, leading to accumulation of inedible palmelloids

Rotifer populations then dropped sharply due to starvation,

relaxing selection against unicells. Finally, the rapid accumula

tion of unicells under relaxed grazing pressures led to the recov-

ery of the rotifer populations (Becks et al. 2010). Therefore, (1)

palmelloid formation confered advantages in the presence of

heavy predation pressure, (2) high proportions of palmelloids

led to predator starvation, relaxing predation pressures for the

entire population, (3) unicellular lineages out-competed palmel-

loid-forming neighbours within the newly established low-

predation environment, and (4) the rise of unicells triggered the

recovery of rotifer populations.

Why don’t terrestrial ecosystems face toxic blooms?

Despite the evidence that emergent public goods may be

important in terrestrial plant and animal communities, TABs

appear to lack obvious terrestrial analogues. Certainly, toxins

have evolved for both offensive and defensive functions

among terrestrial microbes and macrobes, and are central to

the ecological success of many members of these groups. Fur-

thermore, certain elements of TABs may find limited parallels

in plants and animals; for example bark beetle outbreaks

amplify via a positive feedback mediated transition from

targeting small ‘prey’ at low densities, to indiscriminately

overwhelming even the largest and healthiest trees at high

densities (Boone et al. 2011). Invasive plants (particularly

those that employ allelopathy) can rapidly rise to great densi-

ties at the expense of native, susceptible communities (Lankau

2012). Yet, from the perspective of the focal organisms them-




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selves, none of these phenomena appear to match TABs in

terms of spatio-temporal extent or disruptive power across the

functional spectrum of a native community.

It is crucial to delineate the relevant differences between

aquatic and terrestrial communities to appreciate the unique

possibilities for eco-evolutionary feedbacks to shape TAB

dynamics, and to critically assess the utility of TABs as ‘natu-

ral laboratories’ for the study of such dynamics. After all, a

useful model system should offer unique features that are

practically advantageous, without obviously setting it apart

from the less accessible systems that it is intended to model.

We therefore highlight key distinctions between aquatic

(planktonic) systems and their terrestrial (mostly sessile)

counterparts. We focus on those differences with the most

direct relevance to the occurrence of ‘TAB-like’ phenomena,

to the exclusion of many other interesting distinctions that

fundamentally alter the ways in which ecology and evolution

play out on land and in water.

(1) The relative importance of ‘top-down’ vs. ‘bottom-up’

controls on standing photosynthetic biomass. ‘Herbivores

consume far more primary productivity in aquatic than

terrestrial environments (Cyr & Face 1993; Shurin et al.

2006). As a result, the fraction of net primary productivity

accounted for by standing photosynthetic biomass is esti-

mated to be two orders of magnitude lower in aquatic than

terrestrial environments (Polis 1999). Terrestrial plant

communities are thus more likely to be limited by ‘bottom-

up’ controls on growth (e.g. light, space, nutrients). As a

result, the local success of anti-herbivore defences may

have only a minimal impact on standing biomass. In con-

trast, microalgae populations are typically maintained far

below their potential, as defined by bottom-up controls.

Thus, even temporary reductions in grazing rates in a par-

ticular locale (or upon a particular lineage) can lead to

dramatic increases in standing biomass before bottom-up

controls on algae growth take effect.

(2) Mixotrophs are the ultimate resource generalists. Many

bloom-forming microalgae are capable of exploiting

organic and inorganic nutrients, including particulate

material derived from detritus or live prey (Burkholder

et al. 2008). This nutritional flexibility allows mixo-

trophs to avoid (or reduce) reliance upon other popu-

lations or processes. Although terrestrial animals vary

in their degree of specialisation upon different

resources, all must depend on other species to supply

energy (at a minimum). This reliance ultimately limits

the success of any single population, particularly when

exploitation reduces the ability of a favoured resource

to regenerate (as in the case of living resources). ‘Mul-

tichannel’ or ‘subsidised’ omnivores are less strongly

coupled to any one resource, and thus are able to

reduce such limitations to some degree (Polis & Strong

1996). Although land plants are less obviously limited,

their reliance upon inorganic nutrients renders them

dependent on heterotrophic communities for nutrient

cycling. In contrast, mixotrophic algae may be almost

entirely self-reliant for energy production, biosynthesis

and nutrient cycling.5

(3) Random and non-random fluid flow can quickly destroy

and create spatial structure. Many important aspects of an

individual land plant’s habitat remain fixed or change

slowly over its lifetime. In contrast, planktonic microalgae

are constantly drifting, swimming, or being moved by

micro-currents, leading to a highly dynamic local environ-

ment. As a result, the conspecific and heterospecific neigh-

bours of a focal, free-swimming microalga can turn over

relatively rapidly. This latter situation more closely

approximates the assumptions of a simple ‘mean field

model, wherein the average competitive environment

experienced by an individual reflects regional densities of

different species. In terrestrial environments, conspecifics

may cluster together due to endogenous (e.g. limited dis-

persal) or exogenous factors (e.g. patchily distributed

resources). Clustering may limit the success of superior

competitors by increasing the effective (average local) den-

sity of conspecifics, thus amplifying intraspecific competi-

tion (Chesson 2000). Planktonic communities would seem

to lack this type of cross-generational spatial structure

(although colonial species may be a marginal exception),

thus removing an important mechanism of ‘buffering

communities against invasion by superior competitors

voracious predators and virulent pathogens.

Occasionally, however, large-scale advection or strong verti-

cal stratification coupled with phototaxis may cause highly

localised accumulations of previously widely dispersed cells

Such physical processes provide an alternative mechanism of

quickly increasing densities of toxic cells, which does no

involve proliferation. This mechanism appears especially rele

vant to large, slow-reproducing microalgae that typically exist

in sparse populations (e.g. dinoflagellates).Together, these differences may help to explain the apparent

restriction of ‘TAB-like’ phenomena to aquatic systems. How-

ever, the radical demographic changes and profound alterations

to community structure that characterise TABs are not required

for the emergence of public goods, or eco-evolutionary feed-

backs more broadly. In fact, analogous phenomena may well

play out across a range of terrestrial environments. However,

more ‘rigid’ population regulation, continuous (rather than dis-

crete) transitions from private to public effects of beneficia

traits, and longer generation times may all serve to minimise

outward evidence of underlying eco-evolutionary processes in

macroscopic communities.

Biological invasions facilitated by allelopathy provide argu-ably the closest overall terrestrial parallel to the case of TABs

Although they do not approach the disruptive potential of

TABs across functional groups and trophic levels, invasions

by exotic allelopaths can profoundly impact native communi-

ties. Furthermore, the success of invasive populations may

depend largely on costly investments in extra-organismal

compounds, which may function in defensive or competitive

roles. Lankau et al. (2009) found that populations of invasive

annuals invested less in allelochemicals with age (over a scale

5The authors have observed vigorous populations of P. parvum in vials thathad been neglected for almost two years with no inputs except light.




14/17

of decades), which led to declines in the abundances of the

invasive species relative to native competitors. These patterns

are consistent with selection for reduced investment in allelo-

chemicals, despite the importance of this trait for the success

of the population. Furthermore, Lankau (2012) found

evidence that native heterospecific competitors gained resis-

tance to the allelochemicals produced by an invasive plant

over time, allowing them to compete effectively with the

invasive species. Together, these results hint at potentially

deep parallels between invasions of terrestrial ecosystems and

toxic blooms in aquatic environments, underscoring the

possibility for TABs to serve as natural microbial analogues

of important eco-evolutionary dynamics in macroscopic

communities.

Co-evolution and the fate of toxic blooms

Although we have focused primarily on rapid adaptation

within TAB populations, adaptation by other members of

plankton communities in the face of recurrent TABs may

play an important role in bloom dynamics. For exampleDaphnia can quickly evolve resistance in response to blooms

of toxic cyanobacteria (Gustafsson & Hansson 2004;

Hairston et al. 2005; Sarnelle & Wilson 2005), restoring its

ability to exert strong top-down controls on toxic cyanobac-

teria (Chislock et al. 2013). Many TABs harbour significant

populations of apparently resistant heterospecific microalgae

(Michaloudi et al. 2009; Hakanen et al. 2014; Poulson-Elles-

tad et al. 2014), which are unharmed by exposure to high

doses of toxins in the laboratory (Hakanen et al. 2014;

Poulson-Ellestad et al. 2014).

Resistant heterospecific communities may potentially

control the densities of toxic populations via predation and

competition for nutrients, provided they are able to rise tosignificant densities over the course of the bloom. These popu-

lations may therefore reduce the duration and severity of

blooms, particularly in environments subjected to regular

TABs, provided that resistant genotypes persist between

bloom seasons. However, the profoundly non-equilibrium

nature of TABs might prevent (or slow) the accumulation of

resistant lineages in native plankton communities, particularly

if resistance imposes costs during non-TAB conditions

(Hairston et al. 2001). It would be interesting to compare co-

evolution between TAB-forming species and their adversaries

across environments that differ in the regularity with which

TABs occur.

OUTLOOK

The prevalence and importance of eco-evolutionary feedbacks

in nature remains an open question. We have argued that

toxic algal blooms (TABs) are promising candidate natural

laboratories for the study of eco-evolutionary feedbacks in

nature. Our review highlights supporting evidence as well as

open questions and challenges from which the following

research programme can be outlined:

(1) What are the impacts of different environmental pertur-

bations on combined environment and fitness maps? Per-

turbations associated with bloom initiation and

termination may be depicted in an idealised plot of envi-

ronmental and genetic space, as shown in Box 1. For

instance, transient increases (decreases) of toxic cell con-

centrations via abiotic processes (e.g. stratification

hydraulic flushing) may simply increase (decrease) the

‘elevation’ of the population, potentially placing it within

the basin of attraction of a new ecological stable state

Other perturbations are likely to impact both maps; for

instance, nutrient loading may stimulate the growth of

susceptible prey, thus simultaneously increasing popula-

tion density and selection for toxicity. Theoretical work

will be required to systematically determine the effects of

the different ‘types’ of perturbation on TAB populations,

and experimental manipulations in the laboratory (i.e

microcosms) and field (i.e. mesocosms) can be used to

parameterise these models and directly test key predic-

tions.

(2) How do cell-level agents of selection change over the

course of a bloom? There is considerable evidence for

cell-level advantages of toxicity (Table 1); however, these

benefits are rooted in biotic interactions that may be

profoundly impacted by TABs. Key heterospecifics (se-

lective predators and susceptible prey) may decline

develop resistance or persist throughout blooms. These

divergent ecological and evolutionary responses will

determine the balance of private and public effects of

toxicity, and may thus determine the sign and magnitude

of selection for toxigenesis within TABs. The relevance

of private and public goods can be assessed by observa-

tions and manipulations in the field, coupled with labo-

ratory experiments designed to measure the relative

fitness of natural isolates in the presence of different

important heterospecifics.

(3) Do resistant lineages that benefit from TABs contribute

to bloom termination by compromising the public good?

Non-toxic conspecifics and heterospecifics are frequently

isolated from TABs, and in a few cases, these lineages

benefit demonstrably from the presence of toxic strains

(Table 4). Whether these populations act as ‘cheaters’

and undermine the collective benefits of toxigenesis

depends on their indirect effects on toxic populations

The importance of toxicity thresholds (the product of

cell-level toxicity and density of toxic cells) to bloom ini

tiation and collapse suggests that cheaters may play

important and unexplored roles in bloom termination

To our knowledge, this possibility remains entirely unex-

plored, but could be tested directly by manipulating ini-

tial frequencies of toxic and non-toxic microalgae in

mesocosms or microcosms that re-create salient features

of bloom communities.

The answers to these questions have the potential to inform

research into eco-evolutionary feedbacks more broadly

Indeed, we have noted some intriguing parallels between

TABs and other important phenomena, including biologica

invasions of terrestrial plant communities. The relatively con-

spicuous, rapid, and easily manipulated dynamics of TABs

may guide future empirical studies of the roles of mutual




15/17

interactions between ecological and evolutionary change in

more complex ecosystems. More generally, as we face the

pressing question of the scope and limits of biodiversity and

ecosystem adaptation to global change, there is an urgent

need to better understand the role that eco-evolutionary feed-

backs might play in driving catastrophic shifts between alter-

nate ecosystem states. These processes appear to occur

extremely quickly within toxic blooms, providing new oppor-

tunities to directly observe these processes as they play out in

natural environments.

ACKNOWLEDGEMENTS

We thank four anonymous reviewers for their help in

improving this manuscript. We would also like to acknowl-

edge helpful comments from K. Foster on an earlier draft of

this manuscript, and discussions with L.L. Sloat, W.C. Adle,

O.T. Eldakar, J.W. Pepper, J.L. Bronstein, A. Dornhaus,

R.E. Michod, S. de Monte, J.-B.Andre and C. Bowler.

W.W.D. was supported by a “MemoLife” LABEX (ANR-

10-LABX-54) Postdoctoral Fellowship, NSF IOS-1010669and NSF ABI-1262472. R.F. acknowledges funding from the

French Centre National de la Recherche Scientifique

(Pepiniere Interdisciplinaire “Eco-Evo-Devo” de site PSL),

the French Agence Nationale de la Recherche (ANR-09-

PEXT-011 “EVORANGE” and ANR-10 “PHYTBACK”

projects) and the Partner University Fund (collaborative pro-

gramme “Advancing the synthesis of ecology and evolution”

between Ecole Normale Superieure and the University of

Arizona).

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