BACKGROUND: Ecological character displacement is a process of phenotypic differentiation of sympatric populations caused by interspecific competition. Such differentiation could facilitate speciation by enhancing reproductive isolation between incipient species, although empirical evidence for it at early stages of divergence when gene flow still occurs between the species is relatively scarce. Here we studied patterns of morphological variation in sympatric and allopatric populations of two hybridizing species of birds, the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (L. luscinia). RESULTS: We conducted principal component (PC) analysis of morphological traits and found that nightingale species converged in overall body size (PC1) and diverged in relative bill size (PC3) in sympatry. Closer analysis of morphological variation along geographical gradients revealed that the convergence in body size can be attributed largely to increasing body size with increasing latitude, a phenomenon known as Bergmann's rule. In contrast, interspecific interactions contributed significantly to the observed divergence in relative bill size, even after controlling for the effects of geographical gradients. We suggest that the divergence in bill size most likely reflects segregation of feeding niches between the species in sympatry. CONCLUSIONS: Our results suggest that interspecific competition for food resources can drive species divergence even in the face of ongoing hybridization. Such divergence may enhance reproductive isolation between the species and thus contribute to speciation.

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Zobrazit více v PubMed

Brown WL, Wilson EO. Character Displacement. Systematic Zoology. 1956;5:49–64. doi: 10.2307/2411924. DOI

Grant PR. Convergent and divergent character displacement. Biol J Linn Soc. 1972;4:39–68. doi: 10.1111/j.1095-8312.1972.tb00690.x. DOI

Dayan T, Simberloff D. Ecological and community-wide character displacement: The next generation. Ecol Lett. 2005;8:875–894. doi: 10.1111/j.1461-0248.2005.00791.x. DOI

Pfennig KS, Pfennig DW. Character displacement: Ecological and reproductive responses to a common evolutionary problem. Q Rev Biol. 2009;84:253–276. doi: 10.1086/605079. PubMed DOI PMC

Pfennig DW, Pfennig KS. Character displacement and the origins of diversity. Am Nat. 2010;176:26–44. doi: 10.1086/652992. PubMed DOI PMC

Schluter D. Ecological character displacement in adaptive radiation. Am Nat. 2000;156(Supplement):S4–S16.

Fjeldså J. Ecological character displacement and character release in grebes Podicipedidae. Ibis. 1983;125:463–481.

Schluter D. Character displacement and the adaptive divergence of finches on islands and continents. Am Nat. 1988;131:799–824. doi: 10.1086/284823. DOI

Diamond J, Pimm SL, Gilpin ME, Lecroy M. Rapid evolution of character displacement in Myzomelid Honeyeaters. Am Nat. 1989;134:675–708. doi: 10.1086/285006. DOI

Grant PR. Ecology and Evolution of Darwin's Finches. Princeton: Princeton University Press; 1999. PubMed

Benkman CW. Divergent selection drives the adaptive radiation of crossbills. Evolution. 2003;57:1176–1181. PubMed

Grant PR, Grant BR. Evolution of character displacement in Darwin's finches. Science. 2006;313:224–226. doi: 10.1126/science.1128374. PubMed DOI

Coyne JA, Orr HA. Speciation. Sunderland: Sinauer Associates; 2004.

Seddon N. Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution. 2005;59:200–215. PubMed

Kirschel ANG, Blumstein DT, Smith TB. Character displacement of song and morphology in African tinkerbirds. Proc Natl Acad Sci USA. 2009;106:8256–8261. doi: 10.1073/pnas.0810124106. PubMed DOI PMC

Sætre GP, Moum T, Bureš S, Král M, Adamjan M, Moreno J. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature. 1997;387:589–592. doi: 10.1038/42451. DOI

Cody ML. Character convergence. Annu Rev Ecol Syst. 1973;4:189–211. doi: 10.1146/annurev.es.04.110173.001201. DOI

Leary CJ. Evidence of convergent character displacement in release vocalizations of Bufo fowleri and Bufo terrestris (Anura; Bufonidae) Anim Behav. 2001;61:431–438. doi: 10.1006/anbe.2000.1597. DOI

Secondi J, Bretagnolle V, Compagnon C, Faivre B. Species-specific song convergence in a moving hybrid zone between two passerines. Biol J Linn Soc. 2003;80:507–517. doi: 10.1046/j.1095-8312.2003.00248.x. DOI

Jang Y, Won YJ, Choe JC. Convergent and divergent patterns of morphological differentiation provide more evidence for reproductive character displacement in a wood cricket Gryllus fultoni (Orthoptera: Gryllidae) BMC Evol Biol. 2009;9:27. doi: 10.1186/1471-2148-9-27. PubMed DOI PMC

Fox JW, Vasseur DA. Character convergence under competition for nutritionally essential resources. Am Nat. 2008;172:667–680. doi: 10.1086/591689. PubMed DOI

Cody ML. Convergent characteristics in sympatric species: A possible relation to interspecific competition and aggression. Condor. 1969;71:222–239.

Haavie J, Borge T, Bureš S, Garamszegi LZ, Lampe HM, Moreno J, Qvarnström A, Török J, Saetre GP. Flycatcher song in allopatry and sympatry - convergence, divergence and reinforcement. J Evol Biol. 2004;17:227–237. doi: 10.1111/j.1420-9101.2003.00682.x. PubMed DOI

Gorissen L, Gorissen M, Eens M. Heterospecific song matching in two closely related songbirds (Parus major and P. caeruleus): Great tits match blue tits but not vice versa. Behav Ecol Sociobiol. 2006;60:260–269. doi: 10.1007/s00265-006-0164-6. DOI

McDonald DB, Clay RP, Brumfield RT, Braun MJ. Sexual selection on plumage and behavior in an avian hybrid zone: Experimental tests of male-male interactions. Evolution. 2001;55:1443–1451. PubMed

Grant PR, Grant BR, Markert JA, Keller LF, Petren K. Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution. 2004;58:1588–1599. PubMed

Seehausen O, van Alphen JJM, Witte F. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science. 1997;277:1808–1811. doi: 10.1126/science.277.5333.1808. DOI

Ives AR, Boughman JW. Breakdown in postmating isolation and the collapse of a species pair through hybridization. Am Nat. 2010;175:11–26. doi: 10.1086/648559. PubMed DOI

Grant BR, Grant PR. Fission and fusion of Darwin's finches populations. Philos Trans R Soc Lond B. 2008;363:2821–2829. doi: 10.1098/rstb.2008.0051. PubMed DOI PMC

Noor MA. Speciation driven by natural selection in Drosophila. Nature. 1995;375:674–675. doi: 10.1038/375674a0. PubMed DOI

Rundle HD, Schluter D. Reinforcement of stickleback mate preferences: Sympatry breeds contempt. Evolution. 1998;52:200–208. doi: 10.2307/2410935. PubMed DOI

Hoskin CJ, Higgie M, McDonald KR, Moritz C. Reinforcement drives rapid allopatric speciation. Nature. 2005;437:1353–1356. doi: 10.1038/nature04004. PubMed DOI

Silvertown J, Servaes C, Biss P, Macleod D. Reinforcement of reproductive isolation between adjacent populations in the Park Grass Experiment. Heredity. 2005;95:198–205. doi: 10.1038/sj.hdy.6800710. PubMed DOI

Jaenike J, Dyer KA, Cornish C, Minhas MS. Asymmetrical reinforcement and Wolbachia infection in Drosophila. Plos Biol. 2006;4:1852–1862. PubMed PMC

Kronforst MR, Young LG, Gilbert LE. Reinforcement of mate preference among hybridizing Heliconius butterflies. J Evol Biol. 2007;20:278–285. doi: 10.1111/j.1420-9101.2006.01198.x. PubMed DOI

Nosil P, Crespi BJ, Gries R, Gries G. Natural selection and divergence in mate preference during speciation. Genetica. 2007;129:309–327. doi: 10.1007/s10709-006-0013-6. PubMed DOI

Urbanelli S, Porretta D. Evidence of reinforcement of premating isolation between two species of the genus Ochthebius (Coleoptera : Hydraenidae) Evolution. 2008;62:1520–1527. doi: 10.1111/j.1558-5646.2008.00381.x. PubMed DOI

Schluter D. The ecology of adaptive radiation. Oxford: Oxford University Press; 2000.

Price T. Speciation in Birds. Greenwood Village: Roberts & Company Publishers; 2008.

Schluter D, McPhail JD. Ecological character displacement and speciation in sticklebacks. Am Nat. 1992;140:85–108. doi: 10.1086/285404. PubMed DOI

Storchová R, Reif J, Nachman MW. Female heterogamety and speciation: Reduced introgression of the Z chromosome between two species of nightingales. Evolution. 2010;64:456–471. doi: 10.1111/j.1558-5646.2009.00841.x. PubMed DOI PMC

Snow DW, Perrins CM. Birds of Western Palaearctic II. Oxford: Oxford University Press; 1998.

Sorjonen J. Mixed singing and interspecific territoriality: consequences of secondary contact of two ecologically and morphologically similar nightingale species in Europe. Ornis Scand. 1986;17:53–67. doi: 10.2307/3676753. DOI

Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000;405:907–913. doi: 10.1038/35016000. PubMed DOI

Svensson L. Identification guide to European passerines. Norfolk: British Trust for Ornithology; 1992.

Cramp S. The Birds of the Western Palearctic, vol 5. Oxford: Oxford University Press; 1988.

Lille R. Species-specific song and mixed singing of Nightingale and Thrush Nightingale (Luscinia megarhynchos, L. Luscinia) J Ornithol. 1988;129:133–159. doi: 10.1007/BF01647285. DOI

Ranoszek E. Occurrence and habitat preferences in breeding season of the Thrush Nightingale Luscinia luscinia and the Nightingale Luscinia megarhynchos in the Barycz river valley. Ptaki Slaska. 2001;13:19–30.

Becker J. About Nightingales (Luscinia megarhynchos), Trush Nightingales (Luscinia luscinia) and their hybrids - further results of an investigation via bird ringing in the Frankfurt (Oder) area. Vogelwarte. 2007;45:15–26.

Kverek P, Storchová R, Reif J, Nachman MW. Occurrence of a hybrid between the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (Luscinia luscinia) in the Czech Republic confirmed by genetic analysis. Sylvia. 2008;44:17–26.

Stadie C. Erdsanger I; Nachtigall und Sprosser. Europaische Vogelwelt. 1991;3 Sonderheft:130–189.

Goldberg EE, Lande R. Ecological and reproductive character displacement on an environmental gradient. Evolution. 2006;60:1344–1357. PubMed

Adams DC, Collyer ML. Analysis of character divergence along environmental gradients and other covariates. Evolution. 2007;61:510–515. doi: 10.1111/j.1558-5646.2007.00063.x. PubMed DOI

Hagemeijer WJM, Blair MJ. EBCC Atlas of European Breeding Birds. London: T & A D Poyser; 1997.

Jenni L, Winkler R. Moult and aging of European passerines. London: Academic Press; 1994.

Adams DC, West ME, Collyer ML. Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities. J Anim Ecol. 2007;76:289–295. doi: 10.1111/j.1365-2656.2007.01210.x. PubMed DOI

Collyer ML, Adams DC. Analysis of two-state multivariate phenotypic change in ecological studies. Ecology. 2007;88:683–692. doi: 10.1890/06-0727. PubMed DOI

Rice AM, Pfennig DW. Character displacement: in situ evolution of novel phenotypes or sorting of pre-existing variation? J Evol Biol. 2007;20:448–59. doi: 10.1111/j.1420-9101.2006.01187.x. PubMed DOI

Bergmann C. Über die Verhältnisse der Warmeökolomie der Thiere zu ihrer Grösse. Göttinger Studien. 1847;3:595–708. PubMed

Blackburn TM, Gaston KJ, Loder N. Geographic gradients in body size: A clarification of Bergmann's rule. Divers Distribs. 1999;5:165–174. doi: 10.1046/j.1472-4642.1999.00046.x. DOI

Evans KL, Gaston KJ, Sharp SP, McGowan A, Hatchwell BJ. The effect of urbanization on avian morphology and latitudinal gradients in body size. Oikos. 2009;118:251–259. doi: 10.1111/j.1600-0706.2008.17092.x. DOI

Adams DC, Rohlf FJ. Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proc Natl Acad Sci USA. 2000;97:4106–4111. doi: 10.1073/pnas.97.8.4106. PubMed DOI PMC

Rice AM, Leichty AR, Pfennig DW. Parallel evolution and ecological selection: replicated character displacement in spadefoot toads. Proc R Soc B. 2009;276:4189–4196. doi: 10.1098/rspb.2009.1337. PubMed DOI PMC

Huntley B, Green RE, Collingham YC, Willis SG. A Climatic Atlas of European Breeding Birds. Barcelona: Lynx Edicions; 2007.

Gill FB. Ornithology. Third. New York: W.H. Freeman; 2007.

Sedláček O, Fuchs R, Exnerová A. Differences in the nestling diets of sympatric Redstarts Phoenicurus phoenicurus and Black Redstarts P. ochruros: Species-specific preferences or responses to food supply? Acta Ornithol. 2007;42:99–106.

Podos J. A performance constraint on the evolution of trilled vocalization in a songbird family (Passeriformes: Emberizidae) Evolution. 1997;51:537–551. doi: 10.2307/2411126. PubMed DOI

Hoese WJ, Podos J, Boetticher NC, Nowacki S. Vocal tract function in bird song production: Experimental manipulation of beak movements. J Exp Biol. 2000;203:1845–1855. PubMed

Palacios MG, Tubaro PL. Does beak size affect acoustic frequencies in woodcreepers? Condor. 2000;102:553–560. doi: 10.1650/0010-5422(2000)102[0553:DBSAAF]2.0.CO;2. DOI

Podos J. Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature. 2001;409:185–188. doi: 10.1038/35051570. PubMed DOI

Becker J. Sympatric occurrence and hybridization of the Thrush Nightingale (Luscinia luscinia) and the Nightingale (Luscinia megarhynchos) at Frankfurt (Oder), Brandenburg. Vogelwelt. 1995;116:109–118.

Cooley JR. Decoding asymmetries in reproductive character displacement. Proc Acad Nat Sci Phila. 2007;156:89–96. doi: 10.1635/0097-3157(2007)156[89:DAIRCD]2.0.CO;2. DOI

Bednorz J, Kupczyk M, Kuzniak S, Winiecki A. Ptaki Wielkopolski. Poznan: Bogucki Wydawnictwo Naukove; 2000.

Wright S. Evolution in mendelian populations. Genetics. 1931;16:97–159. PubMed PMC

Hey J, Nielsen R. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics. 2004;167:747–760. doi: 10.1534/genetics.103.024182. PubMed DOI PMC

Maynard-Smith J. Evolution and the theory of games. Cambridge: Cambridge University Press; 1982.

Pfennig KS, Pfennig DW. Character displacement as the 'best of a bad situation': fitness trade-offs resulting from selection to minimize resource and mate competition. Evolution. 2005;59:2200–2208. PubMed

Rice AM, Pfennig DW. Does character displacement initiate speciation? Evidence of reduced gene flow between populations experiencing divergent selection. J Evol Biol. 2010;23:854–865. doi: 10.1111/j.1420-9101.2010.01955.x. PubMed DOI

Agrawal AA. Phenotypic plasticity in the interactions and evolution of species. Science. 2001;294:321–326. doi: 10.1126/science.1060701. PubMed DOI

Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP. Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol Evol. 2010;25:459–467. doi: 10.1016/j.tree.2010.05.006. PubMed DOI

Gil D, Bulmer E, Celis P, Lopez-Rull I. Adaptive developmental plasticity in growing nestlings: sibling competition induces differential gape growth. Proc R Soc B. 2008;275:549–554. doi: 10.1098/rspb.2007.1360. PubMed DOI PMC

Heeb P, Schwander T, Faoro S. Nestling detectability affects parental feeding preferences in a cavity-nesting birds. Anim Behav. 2003;66:175–184. doi: 10.1006/anbe.2003.2188. DOI

Pfennig DW, Martin RA. A maternal effect mediates rapid population divergence and character displacement in spadefoot toads. Evolution. 2009;63:898–909. doi: 10.1111/j.1558-5646.2008.00544.x. PubMed DOI

Pfennig DW, Martin RA. Evolution of character displacement in spadefoot toads: different proximate mechanisms in different species. Evolution. 2010;64:2331–2341. PubMed

West-Eberhard MJ. Developmental plasticity and evolution. Oxford: Oxford University Press; 2003.

Darwin C. On the origin of species by means of natural selection. London: Murray; 1859.

Mayr E. Animal species and evolution. Cambridge: Harvard University Press; 1963.

Dieckmann U, Doebeli M. On the origin of species by sympatric speciation. Nature. 1999;400:354–357. doi: 10.1038/22521. PubMed DOI

Doebeli M, Dieckmann U. Speciation along environmental gradients. Nature. 2003;421:259–264. doi: 10.1038/nature01274. PubMed DOI

Polechová J, Barton NH. Speciation through competition: a critical review. Evolution. 2005;59:1194–1210. PubMed

Bolnick DI, Fitzpatrick BM. Sympatric speciation: models and empirical evidence. Annu Rev Ecol Evol Syst. 2007;38:459–487. doi: 10.1146/annurev.ecolsys.38.091206.095804. DOI

Sperm morphology and performance in relation to postmating prezygotic isolation in two recently diverged passerine species

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

Gut microbiota in two recently diverged passerine species: evaluating the effects of species identity, habitat use and geographic distance

3D Geometric Morphometrics Reveals Convergent Character Displacement in the Central European Contact Zone between Two Species of Hedgehogs (Genus Erinaceus)

Postcopulatory sexual selection reduces Z-linked genetic variation and might contribute to the large Z effect in passerine birds

Genomic islands of differentiation in two songbird species reveal candidate genes for hybrid female sterility

Patterns of gene flow and selection across multiple species of Acrocephalus warblers: footprints of parallel selection on the Z chromosome

The causes and evolutionary consequences of mixed singing in two hybridizing songbird species (Luscinia spp.)