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additional species continues, the newconsideration introduced here byFerguson and colleagues [3] is: to whatextent are these developmentalsystems canalized? What novelmechanisms may other species use forensuring the robustness ofdevelopment?
References1. Waddington, C.H. (1942). Canalization of
development and the inheritance of acquiredcharacters. Nature 150, 563–565.
2. Waddington, C.H. (1957). The Strategy of theGenes: A Discussion of Some Aspects ofTheoretical Biology (London: George Allen andUnwin).
3. Gavin-Smyth, J., Wang, Y.-C., Butler, I., andFerguson, E.L. (2013). A genetic networkconferring canalization to a bistable patterningsystem in Drosophila. Curr. Biol. 23,2296–2302.
4. O’Connor, M.B., Umulis, D., Othmer, H.G., andBlair, S.S. (2006). Shaping BMP morphogengradients in the Drosophila embryo and pupalwing. Development 133, 183–193.
5. Eldar, A., Dorfman, R., Weiss, D., Ashe, H.,Shilo, B.Z., and Barkai, N. (2002). Robustnessof the BMP morphogen gradient in Drosophilaembryonic patterning. Nature 419, 304–308.
6. Wang, Y.-C., and Ferguson, E.L. (2005). Spatialbistability of Dpp-receptor interactions duringDrosophila dorsal-ventral patterning. Nature434, 229–234.
7. Umulis, D.M., Serpe, M., O’Connor, M.B., andOthmer, H.G. (2006). Robust, bistablepatterning of the dorsal surface of theDrosophila embryo. Proc. Natl. Acad. Sci. USA103, 11613–11618.
8. Umulis, D.M., Shimmi, O., O’Connor, M.B., andOthmer, H.G. (2010). Organism-scale modelingof early Drosophila patterning via bonemorphogenetic proteins. Dev. Cell 18,260–274.
9. Roth, S. (2011). Mathematics and biology: aKantian view on the history of pattern formationtheory. Dev. Genes Evol. 221, 255–279.
10. Gierer, A., and Meinhardt, H. (1972). A theory ofbiological pattern formation. Kybernetik 12,30–39.
11. Rushlow, C., and Levine, M. (1990). Role of thezerknullt gene in dorsal-ventral patternformation in Drosophila. Adv. Genet. 27,277–307.
12. Wharton, K.A., Ray, R.P., and Gelbart, W.M.(1993). An activity gradient of decapentaplegicis necessary for the specification of dorsalpattern elements in the Drosophila embryo.Development 117, 807–822.
13. Lachaise, D., Harry, M., Solignac, M.,Lemeunier, F., Benassi, V., and Cariou, M.L.(2000). Evolutionary novelties in islands:Drosophila santomea, a new melanogastersister species from Sao Tome. Proc. Biol. Sci.267, 1487–1495.
14. Matute, D.R., Novak, C.J., and Coyne, J.A.(2009). Temperature-based extrinsicreproductive isolation in two species ofDrosophila. Evolution 63, 595–612.
15. Panfilio, K.A. (2008). Extraembryonicdevelopment in insects and the acrobatics ofblastokinesis. Dev. Biol. 313, 471–491.
16. Schmidt-Ott, U., Rafiqi, A.M., and Lemke, S.(2010). Hox3/zen and the evolution ofextraembryonic epithelia in insects. InHox Genes: Studies from the 20th to the21st Century, Volume 689, J.S. Deutsch, ed.(Austin: Landes Bioscience), pp. 133–144.
17. Panfilio, K.A., Oberhofer, G., and Roth, S.(2013). High plasticity in epithelialmorphogenesis during insect dorsal closure.Biol. Open 2, 1108–1118.
18. Rafiqi, A.M., Lemke, S., and Schmidt-Ott, U.(2010). Postgastrular zen expression isrequired to develop distinct amniotic andserosal epithelia in the scuttle fly Megaselia.Dev. Biol. 341, 282–290.
19. Goltsev, Y., Fuse, N., Frasch, M., Zinzen, R.P.,Lanzaro, G., and Levine, M. (2007). Evolution ofthe dorsal-ventral patterning network in themosquito, Anopheles gambiae. Development134, 2415–2424.
20. Rafiqi, A.M., Park, C.-H., Kwan, C.W.,Lemke, S., and Schmidt-Ott, U. (2012). BMP-dependent serosa and amnion specification inthe scuttle fly Megaselia abdita. Development139, 3373–3382.
Institute for Developmental Biology,University of Cologne, Biocenter, ZulpicherStraße 47b, 50674 Koln, Germany.E-mail: [email protected], [email protected]
http://dx.doi.org/10.1016/j.cub.2013.10.073
Evolution: A New Cat SpeciesEmerges
The complex ongoing process of species development is highlighted by thedescription of a new felid species, Leopardus guttulus, from Brazil. Broadmolecular genetic assessments affirm reproductive isolation and separation innature, the hallmark of species recognition.
Stephen J. O’Brien1,2,*and Klaus-Peter Koepfli1
Species recognition used to be simple.A studious naturalist could wanderabout a geographical region to discoverand describe in scholarly detail whatspecies varieties he might encounter.Carl Linnaeus was probably the first todemand some conscious order to theprocess with his Systema Naturaeaffording Latin binomial and trinomialnames to the taxonomyof living species[1]. Charles Darwin added anotherdimension to the process with On theOrigin of Species, which outlined aprocess for creating species diversitythrough adaptation, natural selectionand transition [2]. When paleontologistSteven M. Stanley examined fossildynamics among different species hesuggested that it takes on average 1–2
million years to make new species, atleast among mammals and vertebrates[3]. Recently molecular genetictechniques have weighed in on speciesidentification and taxonomy usingmulti-locus phylogenetic distance,imputed times of divergence amongspecies and a molecular clock asquantifying metrics. Molecular studiesaregenerally concordantwith traditionalmorphological inference, but notalways. As scientists tend to focus onfine-grain details of complex processessuch as speciation, our discussions ofspecies recognition, species transition,species definition and species originshave become complex. In this issueof Current Biology, Tatiane Trigo,Eduardo Eizirik and their colleagues [4]nominate a new species, a small SouthAmerican cat (Figure 1), Leopardusguttulus,previously considered a tigrina
(L. tigrinus), illustrating this complexityquite richly.Why has species pronouncement
become so very controversial? Well,because the term species connotesmany different things. Species are thecurrency of evolution, the endpoint ofa dynamic process, and each species’natural history is distinctive. Theprocess of speciation has becomea discipline of its own with myriadmechanisms documented andconjured up by evolutionary biologists[5,6]. Species definitions areremarkably heterogeneous from thetraditional ‘biological species concept’,which asserts reproductive isolationas the premier distinctive factor[7] compared to phylogenetic,morphological, phenetic, cladistic,and evolutionary species concepts,not to mention subspecies, ESUs(evolutionary significant units), stocksand others subsets, each with varioussurrogate characters of the speciesrecognition proposed. The speciesdefinition controversy is ongoing andhectoring as the ghost of Ernst Mayr,formulator of the biological speciesconcept, haunts all the learnedmonographs. The endless exchangesare reminiscent of U.S. Supreme CourtJustice Potter Stewart’s timeless quip
Figure 1. Leopardus guttulus, the newly recognized cat species from Southeastern Brazil.
Free-ranging individual of Leopardus guttulus photographed with a camera-trap in the AtlanticForest of southern Brazil (Photo: ªProjeto Gatos do Mato, Brazil).
Geoffroy’s cat (Leopardus geoffroyi)
Kodkod (Leopardus guigna)
Tigrina (Leopardus tigrinus)
Andean mountain cat (Leopardus jacobita)
Pampas cat (Leopardus colocolo)
SSE tigrina (Leopardus guttulus)
Margay (Leopardus wiedi)
Ocelot (Leopardus pardalis)
Ocelot ancestor2.9 mya
3 2 1
Current Biology
Figure 2. Family tree of South American cats.
Molecular phylogenetic relationships of cats of the genus Leopardus [20] in South America.
Current Biology Vol 23 No 24R1104
‘‘I shall not attempt to define [hardcorepornography], but I know it when Isee it.’’ Species concepts are equallyelusive, as there is no single correct ortrue answer, only pleas for consensus;hence a plethora of learned treatisesto fuel the stew. Speciation’sintricate details seemingly appear ahodgepodge of dynamic transitioning,yet species remain the units forrecognition in legal aspects of theirprotection and conservation.
Trigo and colleagues [4] provide adetailedanalysisof agroupof small cats(Genus Leopardus; Family Felidae) fromSouth America and offer a snapshot ofthe present state of a complexspeciation process based upon acomprehensive molecular geneticprofiling [4]. Felid zoologiststraditionally recognize a monophyleticgenus, Leopardus, comprising sevenspecies, living today in South andCentral America (Figure 2). The originsof Leopardus, also termed the ocelotlineage, trace back to around 3 millionyears ago when the Americancontinentswere first connected. Prior tothat, South America was drifting aboutthe southern oceans and populatedby diminutive marsupial species,including herbivores, carnivores, andinsectivores. The joining of the twocontinents allowed the ‘Great AmericanInterchange’, a wholesale southwardmigration of placental mammals acrossthe Panamanian isthmus includingsome primitive cats and dogs thathad by that time surpassed marsupialcarnivore counterparts in speed, agility,
ferociousness and predatory acumen[8]. These deadly predators rapidlydisplaced most South Americanmarsupial residents and the catswould gradually evolve into the sevenspecies of the ocelot lineage living theretoday. Trigo et al. [4] have now revisitedthis scenario with compelling data touncover an eighth cryptic new species,Leopardus guttulus. (This name wasoriginally coined as a tigrina subspeciesby Hensel in 1872, and offered asspecies rank by Leyhausen in 1963 [9],but was not generally accepted untilnow).
The new work sampled some 216individual cats from selected localesacross the overlapping ranges ofL. tigrinus (tigrina), L. geoffroyi(Geoffroy’s cat) and L. colocolo(pampas cat). The researchers first
classified the small cats based uponmorphological criteria and thenobtained extensive sequence datafor three gene markers with differentmodes of inheritance (mtDNA, Ychromosome, X chromosome) inaddition to composite genotypes often highly polymorphic short tandemrepeat (STR) or microsatellite loci.Their state-of-the-art
phylogeographic approach revealsseveral conclusions: first, themolecular markers by and largereinforced nicely the notable geneticdistinction between the three studiedLeopardus species with overlappingranges across South America. Second,L. tigrinus parsed into two distinctivepopulations by morphologicalcriteria as well as genotypes. Theanalysis revealed a substantialmolecular genetic distance betweenthe northeastern Brazil tigrinaand south-southeastern tigrinapopulations. The separation theydetected is comparable or greater forall marker modes than differencesamong other long accepted speciesof Leopardus. Hence the authorsconclude that there are actually twomodern species here: L. tigrinus,the northeastern population andsouth-southeastern L. guttulus,adopting the Leyhausen nomenclature[9]. Third, there is considerableevidence of gene flow or hybridizationbetween some but not all of the fourLeopardus species, e.g. bi-directionalamong L. guttulus and L. geoffroyi, butnot between the two traditional tigrinapopulations now dubbed L. tigrinus(northeastern) and L. guttulus(south-southeastern). Cyto-nucleardiscordance, i.e. disagreement of thegroup assignment by nuclear versus
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mitochondrial genotypes, betweenL. tigrinus and L. colocolo likelyreflects relict signatures of ancient,mostly unidirectional gene flow fromL. colocolo to the northeasternL. tigrinus. Cyto-nuclear discordanceis not uncommon among emergingspecies; for example, it is widespreadamong two recently recognized Africanelephant species [10].
There was a time when hybridizationblurred the borders of species andeven muddled the endangeredstatus of species [11]. However,robust documentation of ongoinghybridization, often taking place inhybrid zones but not actually disruptingthe genomic integrity (i.e. retentionof relative genetic distinctiveness),emphasizes that gene flow andhybridization are widespread in nearlyall cases of proto-species rangeoverlap [4,12–14]. Natural processesleading to speciation are not sostraightforward to describe, rather theyare messy, convoluted and sometimesaimless. Transition to reproductiveisolation generally takes quite a fewgenerations to achieve. Perhaps atthe finale of the convoluted process,a proper well-defined species is awonder to perceive.
So what are the physiological orecological mediators of speciesisolation and adaptation? Is not the realpurpose of evolutionary studies, notso much to chronicle but rather tounderstand the adaptive processes ofspecies formation? Trigo et al. [4]offer some plausible suggestions forpossible divergence of L. tigrinus andL. guttulus. The two species diverged0.5 to 0.8 million years ago and todayoccupy distinctive habitats. L. tigrinuslives in dry and open habitats of tropicalsavannahs and shrub lands in centraland northeastern Brazil, known asCerrado and Caatinga, while L. guttulusis found in the more moist AtlanticForests. The radiation of Leopardusspecies shows some fascinatingparallels with the origins of the SouthAmerican fox species of the genusLycalopex having arisen in a similartime and place, with various speciesassociated with distinct geographiesand habitats [15]. Several Lycalopexspecies are also suspected ofhybridizing with each other. Futuregenetic work complemented withelucidating the natural history ofL. tigrinus and L. guttulus will furtherhelp unravel precisely how thesetwo cat species came to be.
The recognition of L. guttulus asthe newest member of the cat familycomes seven years after the cloudedleopard was discovered to comprisetwo genetically and morphologicallydistinct species, Neofelis nebulosa andN. diardi [16,17]. We can also add it tothe list of other recently discoveredNeotropical carnivore species such asthe Eastern mountain coati (Nasuellameridensis) and the olinguito(Bassaricyon neblina) [18,19]. In allthese cases, detailed genetic (and insome cases, morphological) analyseswere used to show that what we oncethought was one species actuallyturned out to be richer indeed.Revealing these patterns is the easypart; understanding the processesbehind them remains a challenge.
References1. Linnaeus, C. (1758). Systema naturae per regna
tria naturae: secundum classes, ordines,genera, species, cum characteribus,differentiis, synonymis, locis (in Latin) (10thed.). Stockholu: Salvirus, L. Dutch classics onHistory of Science. Republished 2003 (Hes &De Graff Pub Br).
2. Darwin, C.R. (1869). On the Origin of Species byMeans of Natural Selection (Cambridge,Harvard University Press).
3. Stanley, S.M. (1980). Macroevolution: Patternand Process. (Baltimore: Johns HopkinsUniversity press).
4. Trigo, T.C., Schneider, A., de Oliveira, T.G.,Lehugeur, L.M., Silveira, L., Freitas, T.R.O., andEizirik, E. (2013). Molecular data reveal complexhybridization and a cryptic species ofNeotropical wild cat. Curr. Biol. 23,2528–2533.
5. Meiri, S., and Mace, G.M. (2007). Newtaxonomy and the origin of species. PLoS Biol.5, e194.
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11. O’Brien, S.J., and Mayr, E. (1991). Bureaucraticmischief: Recognizing endangered species andsubspecies. Science 251, 1187–1188.
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14. Shurtliff, Q.R. (2013). Mammalian hybrid zones:a review. Mammal Rev. 43, 1–21.
15. Wayne, R.K., Van Valkenburgh, B., Kat, P.W.,Fuller, T.K., Johnson, W.E., and O’Brien, S.J.(1989). Genetic and morphological divergenceamong sympatric canids. J. Hered. 80,447–454.
16. Buckley-Beason, V.A., Johnson, W.E.,Nash, W.G., Stanyon, R., Menninger, J.C.,Driscoll, c.A., Howard, J., Bush, M., Page, J.E.,Roelke, M.E., et al. (2006). Molecular Evidencefor Species-Level Distinctions in CloudedLeopards. Curr. Biol. 16, 2371–2376.
17. Kitchener, A.C., Beaumont, M.A., andRichardson, D. (2006). Geographical variation inthe clouded leopard, Neofelis nebulosa, revealstwo species. Curr. Biol. 16, 2377–2383.
18. Helgen, K.M., Kays, R., Helgen, L.E.,Tsuchiya-Jerep, M.T.N., Pinto, C.M.,Koepfli, K.P., Eizirik, E., and Maldonado, J.E.(2009). Taxonomic boundaries and geographicdistributions revealed by an integrativesystematic overview of the mountain coatis,Nasuella (Carnivora: Procyonidae). SmallCarnivore Conservation 41, 65–74.
19. Helgen, K.M., Pinto, M., Kays, R., Helgen, L.,Tsuchiya, M., Quinn, A., Wilson, D., andMaldonado, J. (2013). Taxonomic revision ofthe olingos (Bassaricyon), with description of anew species, the Olinguito. ZooKeys 324, 1–83.
20. Johnson, W.E., Eizirik, E., Pecon-Slattery, J.,Murphy, W.J., Antunes, A., Teeling, E., andO’Brien, S.J. (2006). The late Miocene radiationof modern Felidae: a genetic assessment.Science 311, 73–77.
1Theodosius Dobzhansky Center for GenomeBioinformatics, St. Petersburg StateUniversity, St. Petersburg, 199004, Russia.2Oceanographic Center Nova SoutheasternUniversity, Ft Lauderdale, Florida 33004,USA.*E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2013.10.074
Meiosis: Cohesin’s Hidden Role in theCheckpoint Revealed
The spindle assembly checkpoint prevents aneuploidy by ensuring thatchromosomes are properly distributed during cell division. A new study showsthat the integrity of the checkpoint response depends on centromeric cohesinin mammalian oocytes.
So I. Nagaoka
When a cell divides, it is vital that all ofits genetic information is equally
inherited by the two daughter cells.This is because aneuploidy (a gain orloss of chromosomes) resulting fromunequal distribution of the genetic
