Skip to main content

Advertisement

Log in

Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Recent advances in morphometrics and genetics have led to the discovery of numerous cryptic species in coral reef ecosystems. A prime example is the Montastraea annularis scleractinian coral species complex, in which morphological, genetic, and reproductive data concur on species boundaries, allowing evaluation of long-term patterns of speciation and evolutionary innovation. Here we test for cryptic species in the Atlantic species, Montastraea cavernosa, long recognized as polymorphic. Our modern samples consist of 94 colonies collected at four locations (Belize, Panamá, Puerto Rico in the Caribbean; São Tomé in the Eastern Atlantic). Our fossil samples consist of 78 colonies from the Plio-Pleistocene of Costa Rica and Panamá. Landmark morphometric data were collected on thin sections of 46 modern and 78 fossil colonies. Mahalanobis distances between colonies were calculated using Bookstein coordinates, revealing two modern and four fossil morphotypes. The remaining 48 of the 94 modern colonies were assigned to morphotype using discriminant analysis of calical measurements. Cross-tabulation and multiple comparisons tests show no significant morphological differences among geographic locations or water depths. Patterns of variation within and among fossil morphotypes are similar to modern morphotypes. DNA sequence data were collected for two polymorphic nuclear loci -tub1 and β-tub2) on all 94 modern colonies. Haplotype networks show that both genes consist of two clades, but morphotypes are not associated with genetic clades. Genotype frequencies and two-locus genotype assignments indicate genetic exchange across clades, and ϕst values show no genetic differentiation between morphotypes at different locations. Taken together, our morphological and genetic results do not provide evidence for cryptic species in M. cavernosa, but indicate instead that this species has an unusually high degree of polymorphism over a wide geographic area and persisting for >25 million years (myr).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Acosta A, Zea S (1997) Sexual reproduction of the reef coral Montastrea cavernosa (Scleractinia: Faviidae) in the Santa Marta area, Caribbean coast of Colombia. Mar Biol 128:141–148

    Article  Google Scholar 

  • Barroso R, Klautau M, Sole-Cava AM, Paiva PC (2010) Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Mar Biol 157:69–80

    Article  Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    Article  PubMed  CAS  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, Cambridge 435 p

    Google Scholar 

  • Brazeau DA, Gleason DF, Morgan ME (1998) Self-fertilization in brooding hermaphroditic Caribbean corals: evidence from molecular markers. J Exp Mar Biol Ecol 231:225–238

    Article  Google Scholar 

  • Budd AF (1991) Neogene Paleontology in the Northern Dominican Republic. 11. The Family Faviidae (Anthozoa: Scleractinia). Part I. Bull AmPaleontol 101(338):5–83, pls. 1–29

  • Budd AF (1993) Variation within and among morphospecies of Montastraea. Courier Forschungs-institut Senckenberg 164:241–254

    Google Scholar 

  • Budd AF, Johnson KG (1999) Origination preceding extinction during Late Cenozoic turnover of Caribbean reefs. Paleobiology 25:188–200

    Google Scholar 

  • Budd AF, Klaus JS (2001) The origin and early evolution of the Montastraea “annularis” species complex (Anthozoa: Scleractinia). J Paleontol 75:527–545

    Article  Google Scholar 

  • Budd AF, Klaus JS (2008) Early evolution of the Montastraea “annularis” species complex (Anthozoa: Scleractinia): Evidence from the Mio-Pliocene of the Dominican Republic. In: Nehm RH, Budd AF (eds) Evolutionary stasis and change in the Dominican Republic Neogene. Springer, New York, pp 85–124

    Chapter  Google Scholar 

  • Budd AF, Pandolfi JM (2004) Overlapping species boundaries and hybridization within the Montastraea “annularis” reef coral complex in the Pleistocene of the Bahama Islands. Paleobiology 30:396–425

    Article  Google Scholar 

  • Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of species distributions. Science 328:1558–1561

    Article  PubMed  CAS  Google Scholar 

  • Budd AF, Stemann TA, Stewart RH (1992) Eocene Caribbean reef corals: a unique fauna from the Gatuncillo Formation of Panama. J Paleontol 66:570–594

    Google Scholar 

  • Budd AF, Stemann TA, Johnson KG (1994) Stratigraphic distributions of genera and species of Neogene to Recent Caribbean reef corals. J Paleontol 68:951–977

    Google Scholar 

  • Budd AF, Johnson KG, Stemann TA, Tompkins BH (1999) Pliocene to Pleistocene reef coral assemblages in the Limon Group of Costa Rica. In: Collins LS, Coates AG (eds), A Paleobiotic Survey of the Caribbean Faunas from the Neogene of the Isthmus of Panama. Bulletins of American Paleontology, Special Volume 357:119–158

  • Calvo M, Templado J, Oliverio M, Machordom A (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biol J Linn Soc 96:898–912

    Article  Google Scholar 

  • Carpenter KE and 38 others (2008) One-third of reef building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Google Scholar 

  • Chen IP, Tang CY, Chiou CY et al (2009) Comparative analyses of coding and noncoding DNA regions indicate that Acropora (Anthozoa: Scleractina) possesses a similar evolutionary tempo of nuclear vs. mitochondrial genomes as in plants. Mar Biotechnol 11:141–152

    Article  PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Coates AG, McNeill DF, Aubry M-P, Berggren WA, Collins LS (2005) An introduction to the geology of the Bocas del Toro Archipelago, Panama. Caribb J Sci 41:374–391

    Google Scholar 

  • Collins LS, Coates AG (eds) (1999) A Paleobiotic Survey of Caribbean Faunas from the Neogene of the Isthmus of Panama. Bull Am Paleontol 357:351

  • Diekmannn OE, Bak RPM, Stam WT, Olsen JL (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar Biol 139:221–233

    Article  Google Scholar 

  • Duncan PM (1863) On the fossil corals of the West Indian Islands. Part 1. Q J Geol Soc Lond 20:406–458, pls 13–16

    Google Scholar 

  • Eldredge N, Gould SJ (1972) Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf TJM (ed) Models in paleobiology. Freeman Cooper, San Francisco, pp 82–115

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1

  • Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389

    Article  PubMed  CAS  Google Scholar 

  • Flot J, Magalon H, Cruard C, Couloux A, Tillier S (2008) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biol 331:239–247

    Article  Google Scholar 

  • Forsman ZH, Guzman HM, Chen CA, Fox GE, Wellington GM (2005) An ITS region phylogeny of Siderastrea (Cnidaria:Anthozoa): is S. glynni endangered or introduced? Coral Reefs 24:343–347

    Article  Google Scholar 

  • Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ (2009) Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9:45

    Article  PubMed  Google Scholar 

  • Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004a) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337

    PubMed  CAS  Google Scholar 

  • Fukami H, Budd AF, Paulay G, Solé-Cava A, Chen CA, Iwao K, Knowlton N (2004b) Conventional Taxonomy Obscures Deep Divergence between Pacific and Atlantic Corals. Nature 427:832–835

    Article  PubMed  CAS  Google Scholar 

  • Fukami H, Chen CA, Budd AF, Collins A, Wallace C, Chuang Y-Y, Chen C, Dai C-F, Iwao K, Sheppard C, Knowlton N (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS One 3(9):e3222(1–9)

    Article  Google Scholar 

  • Gillespie JH (2004) Population genetics: a concise guide, 2nd edn. The Johns Hopkins University Press, Baltimore 232 pp

    Google Scholar 

  • Goodbody-Gringley G, Vollmer SV, Woollacott RM, Giribet G (2010) Limited gene flow in the brooding coral Favia fragum (Esper, 1797). Marine Biology. doi:10.1007/s00227-00010-01521-00226

  • Goreau TF (1959) The ecology of Jamaican coral reefs. I. Species composition and zonation. Ecology 40:67–90

    Article  Google Scholar 

  • Goreau TF, Wells JW (1967) The shallow-water Scleractinia of Jamaica: revised list of species and their vertical distribution range. Bull Mar Sci 17:442–453

    Google Scholar 

  • Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24

    Article  PubMed  Google Scholar 

  • Hunt G (2007) The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proc Natl Acad Sci 104:18404–18408

    Article  PubMed  CAS  Google Scholar 

  • Jablonski D (2007) Scale and hierarchy in macroevolution. Palaeontology 50:87–109

    Article  Google Scholar 

  • Jackson JBC, Cheetham AH (1990) Evolutionary significance of morphospecies; a test with cheilostome Bryozoa. Science 248:579–583

    Article  PubMed  CAS  Google Scholar 

  • Jackson JBC, Cheetham AH (1999) Tempo and mode of speciation in the sea. Trends Ecol Evol 14:72–77

    Article  PubMed  Google Scholar 

  • Johnson KG (2001) Middle Miocene recovery of Caribbean reef corals: new data from the Tamana Formation of Trinidad. J Paleontol 75:513–526

    Article  Google Scholar 

  • Johnson KG (2007) Reef-coral diversity in the Late Oligocene Antigua Formation and temporal variation of local diversity on Caribbean Cenozoic Reefs. In: Hubmann B, Piller WE (eds) Fossil Corals and Sponges. Proceedings of the 9th International Symposium on Fossil Cnidaria and Porifera. Österr. Akad. Wiss., Schriftenr. Erdwiss. Komm. 17:471–491, 1 Tab., 5 Figs., 2 Pls., Wien

  • Johnson KG, Kirby MX (2006) The Emperador Limestone rediscovered: Early Miocene corals from the Culebra Formation, Panama. J Paleontol 80:283–293

    Article  Google Scholar 

  • Klaus JS, Budd AF, Heikoop JM, Fouke BW (2007) Environmental controls on corallite morphology in the reef coral Montastraea annularis. Bull Mar Sci 80:233–260

    Google Scholar 

  • Klaus JS, Budd AF, Johnson KG, McNeill DF (2008) Assessing community change in Miocene to Pliocene coral assemblages of the northern Dominican Republic. In: Nehm RH, Budd AF (eds) Evolutionary stasis and change in the Dominican Republic Neogene. Springer, New York, pp 193–224

    Chapter  Google Scholar 

  • Klautau M, Russo CAM, Lazoski C et al (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53:1414–1422

    Article  Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologica 420:73–90

    Article  CAS  Google Scholar 

  • Knowlton N, Budd AF (2001) Recognizing coral species past and present. In: Jackson JBC, Lidgard S, McKinney FK (eds) Evolutionary patterns: growth, form, and tempo in the fossil record. Univ. Chicago Press, Chicago, pp 97–119

    Google Scholar 

  • Knowlton N, Jackson JBC (1994) New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends Ecol Evol 9:7–9

    Article  PubMed  CAS  Google Scholar 

  • Knolwton N, Weil E, Weigt LA, Guzman HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330–333

    Article  Google Scholar 

  • Laborel J (1969) Madréporaires et Hydrocoralliaires récifaux des côtes brésiliiennes. Annales del Institute Océanographique 47:171–229, 8 pls

  • Laborel J (1974) West African reefs corals: an hypothesis on their origin. Proceedings of the 2nd International Coral Reef Symposium 1: 425–443

  • Lasker HR (1976) Intraspecific variability of zooplankton feeding in the hermatypic coral Montastraea cavernosa. In: Mackie GW (ed) Coelenterate ecology and behavoir. Plenum Press, New York, pp 101–109

    Google Scholar 

  • Lasker HR (1979) Light dependent activity patterns among reef corals: Montastraea cavernosa. Biol Bull 156:196–211

    Article  Google Scholar 

  • Lasker HR (1980) Sediment rejection by reef corals: the roles of behavior and morphology in Montastraea cavernosa (Linnaeus). J Exp Mar Biol Ecol 47:77–87

    Article  Google Scholar 

  • Lasker HR (1981) Phenotypic variation in the coral Montastraea cavernosa and its effects on colony energetics. Biol Bull 160:292–302

    Article  Google Scholar 

  • Lee T, Foighil DO (2005) Placing the Floridian marine genetic disjunction into a regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex. Evolution 59:2139–2158

    PubMed  CAS  Google Scholar 

  • Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323

    PubMed  Google Scholar 

  • Lin HC, Sanchez-Ortiz C, Hastings PA (2009) Colour variation is incongruent with mitochondrial lineages: cryptic speciation and subsequent diversification in a Gulf of California reef fish (Teleostei: Blennioidei). Mol Ecol 18:2476–2488

    Article  PubMed  CAS  Google Scholar 

  • Linneaus C (1767) Madrepora. Systema Naturae, Holmiae, Editio Duodecima, Reformata, t.1, pt.2, pp 1272–1282

  • Mathews LM (2006) Cryptic biodiversity and phylogeographical patterns in a snapping shrimp species complex. Mol Ecol 15:4049–4063

    Article  PubMed  CAS  Google Scholar 

  • McNeill DF, Coates AG, Budd AF, Borne PF (2000) Integrated paleontologic and paleomagnetic stratigraphy of the upper Neogene deposits around Limon, Costa Rica: a coastal emergence record of the Central American Isthmus. Geol Soc Am Bull 112:963–981

    Article  CAS  Google Scholar 

  • Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus Platygyra. Bull Mar Sci 61:907–917

    Google Scholar 

  • Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572

    Article  PubMed  CAS  Google Scholar 

  • Nunes F (2009) Biodiversity and connectivity in peripheral populations of corals of the South and Eastern Atlantic. PhD Dissertation, University of California, San Diego, 142 pp

  • Nunes F, Fukami H, Vollmer SV, Norris RD, Knowlton N (2008) Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs 27:423–432

    Article  Google Scholar 

  • Nunes F, Norris RD, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18:4283–4297

    Article  PubMed  CAS  Google Scholar 

  • Pandolfi JM, Budd AF (2008) Morphology and ecological zonation of Caribbean reef corals: the Montastraea ‘annularis’ species complex. Mar Ecol Prog Ser 369:89–102

    Article  Google Scholar 

  • Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) The phylogeography and connectivity of the latitudinally widespread scleractinian coral Plesiastrea versipora in the Western Pacific. Mol Ecol 11:1177–1189

    Article  PubMed  CAS  Google Scholar 

  • Ruiz H (2004). Morphometric examination of corallite and colony variability in the Caribbean coral Montastraea cavernosa (Linnaeus 1766). Ms.C Thesis (Advisor Dr. Ernesto Weil). Department of Marine Sciences, University of Puerto Rico Mayaguez, 79 pp

  • Schultz HA, Budd AF (2008) Neogene evolution of the reef coral species complex Montastraea “cavernosa”. In: Nehm RH, Budd AF (eds) Evolutionary stasis and change in the Dominican Republic Neogene. Springer, New York, pp 147–170

    Chapter  Google Scholar 

  • Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68

    Article  Google Scholar 

  • Shearer TL, Van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  CAS  Google Scholar 

  • Sterrer W (ed) (1986) Marine fauna and flora of Bermuda. Wiley, New York 774 pp

    Google Scholar 

  • Szmant AM (1986) Reproductive ecology of Caribbean Reef Corals. Coral Reefs 5:43–53

    Article  Google Scholar 

  • Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastraea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25

    Article  Google Scholar 

  • Szmant AM, Weil E, Miller MW, Colon DE (1996) Hybridization in the species complex of Montastraea annularis. Mar Biol 129:561–572

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337

    Article  PubMed  Google Scholar 

  • Vaughan TW (1919) Fossil corals from Central America, Cuba, and Porto Rico with an account of the American Tertiary, Pleistocene, and recent coral reefs. U.S. National Museum Bulletin 103:189–524, pls. 68–152

  • Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol Ecol 13:2763–2772

    Article  PubMed  CAS  Google Scholar 

  • Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: Implications for the recovery of endangered reefs. J Hered 98:40–50

    Article  PubMed  CAS  Google Scholar 

  • Wei NV, Wallace CC, Dai CF, Pillay RM, Chen CA (2006) Analyses of the Ribosomal Internal Transcribed Spacers (ITS) and the 5.8S Gene Indicate that Extremely High rDNA Heterogeneity is a Unique Feature in the Scleractinian Cora Genus Acropora (Scleractinia;Acroporidae). Zool Stud 45(3):404–418

    CAS  Google Scholar 

  • Weil E, Knowlton N (1994) A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis & Solander, 1786) and its two sibling species, M. faveolata (Ellis & Solander, 1786), and M. franksi (Gregory, 1895). Bull Mar Sci 54(3):151–175

    Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Finks WL (2004) Geometric morphometrics for biologists: a primer. Elsevier, Amsterdam, 416 p

    Google Scholar 

Download references

Acknowledgments

We thank Myra Laird (University of Iowa) and Jonathan Lee (University of California, San Diego) for photography and measuring specimens, and Matthew Wortel (University of Iowa Geoscience Petrographic Facilities) for preparing thin sections. Diving assistance in Belize was provided by Claudia and Dan Miller. David Anderson assisted with specimen collection and morphological measurements in Puerto Rico. Nancy Knowlton and Richard Norris provided helpful comments and discussions. This research was supported by a grant from the US National Science Foundation Grant [DEB-0343208 to AFB], a doctoral fellowship from the Center of Marine Biodiversity and Conservation [to FN], the John Dove Isaacs Chair in Natural Philosophy [to N. Knowlton], the Department of Marine Sciences, University of Puerto Rico [to EW], and both the Australian Research Council Centre of Excellence for Coral Reef Studies and the Smithsonian Institution’s Marine Science Network grants [to JMP].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ann F. Budd.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 431 kb)

Figure S1

(a) Phylogenetic trees based on β-tub1 inferred by neighbor-joining (left) and maximum parsimony (right) methods implemented in MEGA. Bootstrap support >0.50 isreported (branches with <0.50 support have been collapsed). Haplotype names are precededby their Clade assignment (A or B). (b) Phylogenetic trees based on β-tub2 inferred byneighbor-joining (left) and maximum parsimony (right) methods implemented in MEGA.Bootstrap support >0.50 is reported (branches with <0.50 support have 995 been collapsed). Haplotype names are preceded by their Clade assignment (C or D)(JPG 1927 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Budd, A.F., Nunes, F.L.D., Weil, E. et al. Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications. Evol Ecol 26, 265–290 (2012). https://doi.org/10.1007/s10682-010-9460-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-010-9460-8

Keywords

Navigation