Abstract
Animal hybridization is increasingly recognized as common and evolutionarily important, but the role of behavior in promoting hybridization events is not well understood. Understanding the behavioral causes of hybridization requires understanding the ecological, demographic, and phenotypic influences on mate choice in hybridizing taxa. Here, I review how these influences on mate choice can contribute to hybridization by (1) circumventing (female) choice, (2) bringing formerly isolated species into sympatry, (3) masking cues important for mate recognition, (4) altering the traits or preferences involved in mate recognition, or (5) altering the costs and benefits of mate choice. In particular, hybridization in response to either high direct costs of mate choice or high direct benefits of heterospecific mating may be widespread, a possibility that awaits further testing. Adopting a mate choice perspective to the study of hybridization challenges the assumption of hybrids as reproductive “mistakes” and allows for functional explanations regarding the occurrence and maintenance of hybridization. As evidence of the prevalence and evolutionary importance of animal hybridization accumulates, investigations into the role of behavior will be increasingly important for our understanding of diversification and for conservation applications.
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References
Allendorf FW, Leary RF (1988) Conservation and distribution of genetic variation in a polytypic species, the cutthroat trout. Cons Biol 2:170–184
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problem with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford
Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10:67–71
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Avise JC, Saunders NC (1984) Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics 108:237–255
Bank C, Hermisson J, Kirkpatrick M (2012) Can reinforcement complete speciation? Evolution 66:229–239
Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Evol Syst 16:113–148
Basolo AL (1990) Female preference for male sword length in the green swordtail, Xiphophorus helleri (Pisces: Poeciliidae). Anim Behav 40:332–338
Bateson P (ed) (1983) Mate choice. Cambridge University Press, Cambridge
Blair AP (1941) Variation, isolating mechanisms, and hybridization in certain toads. Genetics 26:398–417
Bolnick DI (2004) Waiting for sympatric speciation. Evolution 58(4):895–899
Brodsky LM, Weatherhead PJ (1984) Behavioral and ecological factors contributing to American black duck-mallard hybridization. J Wildlife Manage 48(3):846–852
Brodsky LM, Ankney CD, Dennis DG (1988) The influence of male dominance on social interactions in black ducks and mallards. Anim Behav 36:1371–1378
Campton DE (1987) Natural hybridization and introgression in fishes: methods of detection and genetic interpretations. In: Ryman N, Utter F (eds) Population genetics and fishery management. University of Washington Press, Seattle, pp 161–192
Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Current Biol 16(17):R755–R765
Coyne JA, Orr HA (1997) “Patterns of speciation in Drosophila” revisited. Evolution 51:295–303
Coyne JA, Orr HA (2004) Speciation. Sunderland Associates Inc., Sunderland
Darwin CR (1861) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 3rd edn. John Murray, London
delBarco-Trillo J, McPhee ME, Johnston RE (2010) Adult female hamsters avoid interspecific mating after exposure to heterospecific males. Behav Ecol Sociobiol 64:1247–1253
d'Udine B, Alleva E (1983) Early experience and sexual preferences in rodents. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 311–327
Dukas R (2004) Male fruit flies learn to avoid interspecific courtship. Behav Ecol 15:695–698
Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654
Espinedo CM, Gabor CR, Aspbury AS (2010) Males, but not females, contribute to sexual isolation between two sympatric species of Gambusia. Evol Ecol 24:865–878
Feldhaar H, Foitzik S, Heinze J (2008) Lifelong commitment to the wrong partner: hybridization in ants. Phil Trans R Soc B 363:2891–2899
Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc B 273:1187–1193
Garcia-Vazquez E, Moran P, Perez J, Martinez JL, Izquierdo JI, de Gaudemar B, Beall E (2002) Interspecific barriers between salmonids when hybridisation is due to sneak mating. Heredity 89:288–292
Gee JM (2003) How a hybrid zone is maintained: behavioral mechanisms of interbreeding between California and Gambel's quail (Callipepla californica and C. gambelii). Evolution 57:2407–2415
Gerlai R (2007) Mate choice and hybridization in Lake Malawi cichlids, Sciaenochromis fryeri and Cynotilapia afra. Ethology 113:673–685
Good TP, Ellis JC, Annett CA, Pierotti R (2000) Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54:1774–1783
Grant PR, Grant BR (1992) Hybridization of bird species. Science 256(5054):193–197
Grant BR, Grant PR (1993) Evolution of Darwin's finches caused by a rare climatic event. Proc R Soc B 251:111–117
Grant PR, Grant BR (1997) Hybridization, sexual imprinting, and mate choice. Am Nat 149(1):1–28
Grant PR, Grant BR, Keller LF, Markert JA, Petren K (2003) Inbreeding and interbreeding in Darwin's finches. Evolution 57:2911–2916
Grant PR, Grant BR, Markert JA, Keller LF, Petren K (2004) Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution 58(7):1588–1599
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282
Hebets EA (2003) Subadult experience influences adult mate choice in an arthropod: exposed female wolf spiders prefer males of a familiar phenotype. Proc Natl Acad Sci USA 100:13390–13395
Hebets EA, Vink CJ (2007) Experience leads to preference: experienced females prefer brush-legged males in a population of syntopic wolf spiders. Behav Ecol 18:1010–1020
Herrington SJ, Hettiger KN, Heist EJ, Keeney DB (2008) Hybridization between longnose and alligator gars in captivity, with comments on possible gar hybridization in nature. Trans Amer Fish Soc 137:158–164
Hettyey A, Baksay S, Vági B, Hoi H (2009) Counterstrategies by female frogs to sexual coercion by heterospecifics. Anim Behav 78:1365–1372
Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20
Izzo AS, Gray DA (2011) Heterospecific courtship and sequential mate choice in sister species of field crickets. Anim Behav 81:259–264
Jennings MJ, Philipp DP (2002) Alternative mating tactics in sunfishes (Centrarchidae): a mechanism for hybridization? Copeia 2002:1102–1105
Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327
Jones IL, Hunter FM (1998) Heterospecific mating preferences for a feather ornament in least auklets. Behav Ecol 9:187–192
Jouventin P, Bried J (1997) The effect of mate choice on speciation in snow petrels. Biol Rev 72:283–327
Kendrick KM, Hinton MR, Atkins K, Haupt MA, Skinner JD (1998) Mothers determine sexual preferences. Nature 395:229–230
Kirkpatrick M (1996) Good genes and direct selection in evolution of mating preferences. Evolution 50:2125–2140
Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mate preferences. Proc Natl Acad Sci USA 94:1282–1286
Kitano S, Maekawa K, Nakano S, Fausch KD (1994) Spawning behavior of bull trout in the Upper Flathead Drainage, Montana, with special reference to hybridization with brook trout. Trans Amer Fish Soc 123:933–992
Kopp M, Hermisson J (2008) Competitive speciation and costs of choosiness. J Evol Biol 21:1005–1023
Kozak GM, Reisland M, Boughman JW (2009) Sex differences in mate recognition and conspecific preference in species with mutual mate choice. Evolution 63:353–365
Kozak GM, Head ML, Boughman JW (2011) Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks. Proc R Soc B 278:2604–2610
Lemaire F (1977) Mixed song, interspecific competition and hybridisation in the reed and marsh warblers (Acrocephalus scirpaceus and palustris). Behaviour 63:215–240
Lengagne T, Grolet O, Joly P (2006) Male mating speed promote hybridization in the Rana lessonae–Rana esculenta waterfrog system. Behav Ecol Sociobiol 60:123–130
Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699
Magurran AE, Ramnarine IW (2004) Learned mate recognition and reproductive isolation in guppies. Anim Behav 67:1077–1082
Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45:331–355
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237
Mallet J (2007) Hybrid speciation. Nature 446:279–283
Marshall VT, Schwartz JJ, Gerhardt HC (2006) Effects of heterospecific call overlap on the phonotactic behaviour of grey treefrogs. Anim Behav 72:449–459
Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge
Mayr E (1970) Populations, species and evolution: an abridgment of Animal species and evolution. Belknap Press, Cambridge
McCarthy E (2006) Handbook of avian hybrids of the world. Oxford University Press, New York
Mendelson TC, Shaw KL (2012) The (mis)concept of species recognition. Trends Ecol Evol 27:421–427
Miller EH, Ponce de León A, DeLong RL (1996) Violent interspecific sexual behavior by male sea lions (Otariidae): evolutionary and phylogenetic implications. Mar Mamm Sci 12:468–476
Moore JA (1957) An embryologist's view of the species concept. In: Mayr E (ed) The species problem. American Association for the Advancement of Science, Washington, DC, pp 325–338
Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–277
Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–218
Nomakuchi S, Higashi K (1996) Competitive habitat utilization in the damselfly, Mnais nawai (Zygoptera: Calopterygidae) coexisting with a related species, Mnais pruinosa. Res Popul Ecol 38:41–50
Noor MAF (1996) Absence of species discrimination in Drosophila pseudoobscura and D. persimilis males. Anim Behav 52:1205–1210
Nuechterlein GL, Buitron D (1998) Interspecific mate choice by late-courting male western grebes. Behav Ecol 9(3):313–321
Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NB (eds) Sexual selection and reproductive competition in insects. Academic Press, New York
Parker GA, Partridge L (1998) Sexual conflict and speciation. Phil Trans R Soc Lond B 353:261–274
Paterson HEH (1985) The recognition concept of species. In: Vrba ES (ed) Species and speciation. Transvaal Museum, Pretoria, pp 21–29
Peterson MA, Honchak BM, Locke SE, Beeman TE, Mendoza J, Green J, Buckingham KJ, White MA, Monsen KJ (2005) Relative abundance and the species-specific reinforcement of male mating preference in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone. Evolution 59:2639–2655
Pfennig KS (2000) Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav Ecol 11:220–227
Pfennig KS (2007) Facultative mate choice drives adaptive hybridization. Science 318:965–967
Pierotti R, Annett CA (1993) Hybridization and male parental investment in birds. Condor 95:670–679
Price TD, Bouvier MM (2002) The evolution of F-1 postzygotic incompatibilities in birds. Evolution 56:2083–2089
Qvarnström A, Haavie J, Sæther SA, Eriksson D, Pärt T (2006) Song similarity predicts hybridization in flycatchers. J Evol Biol 19:1202–1209
Randler C (2002) Avian hybridization, mixed pairing and female choice. Anim Behav 63:103–119
Randler C (2004) Frequency of bird hybrids: does detectability make all the difference? J Ornithol 145:123–128
Randler C (2005) Do forced extrapair copulations and interspecific brood amalgamation facilitate natural hybridisation in wildfowl? Behaviour 142:477–488
Randler C (2006) Behavioural and ecological correlates of natural hybridization in birds. Ibis 148(3):459–467
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109
Rhymer JM, Williams MJ, Braun MJ (1994) Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk 111:970–978
Ribi G, Oertli S (2000) Frequency of interspecific matings and of hybrid offspring in sympatric populations of Viviparus ater and V. contectus (Mollusca: Prosobranchia). Biol J Linn Soc 71:133–143
Ribi G, Porter AH (1995) Mating between two hybridizing species, Viviparus ater and V. contectus (Mollusca: Prosobranchia). Anim Behav 49:1389–1398
Risch M, Andersen L (1998) Selektive partnerwahl der aaskrähe (Corvus corone) in der hybridisierungszone von rabenkrähe (C. c. corone) und nebelkrähe (C. c. cornix). J Ornithol 139:173–177
Rohwer S (1994) Two new hybrid Dendroica warblers and new methodology for inferring parental species. Auk 111:441–449
Rosenfield JA, Kodric-Brown A (2003) Sexual selection promotes hybridization between Pecos pupfish, Cyprinodon pecosensis and sheepshead minnow, C. variegatus. J Evol Biol 16:595–606
Ryan MJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657
Ryan MJ, Wagner WE (1987) Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science 236(4801):595–597
Schlupp I, Marler C, Ryan MJ (1994) Benefit to male sailfin mollies of mating with heterospecific females. Science 21:373–374
Schmeller DS, O'Hara R, Kokko H (2005) Male adaptive stupidity: male mating pattern in hybridogenetic frogs. Evol Ecol Res 7:1039–1050
Schwenk K, Brede N, Streit B (2008) Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Phil Trans R Soc B 363:2805–2811
Secondi J, Johanet A, Pays O, Cazimajou F, Djalout Z, Lemaire C (2010) Olfactory and visual species recognition in newts and their role in hybridization. Behaviour 147:1693–1712
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Seehausen O, van Alphen JJM (1998) The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behav Ecol Sociobiol 42:1–8
Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811
Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44
Seymour NR (1990) Forced copulations in sympatric American black ducks and mallards in Nova Scotia. Can J Zool 68:1691–1696
Sullivan BK (2009) Mate recognition, species boundaries and the fallacy of “species recognition”. Open Zool J 2:86–90
Svensson EI, Eroukhmanoff F, Karisson K, Runemark A, Brodin A (2010) A role for learning in population divergence of mate preferences. Evolution 64:3101–3113
ten Cate C, Bateson PPG (1988) Sexual selection: the evolution of conspicuous characteristics in birds by means of imprinting. Evolution 42:1355–1358
Turelli M, Begun DJ (1997) Haldane's Rule and X-chromosome Size in Drosophila. Genetics 147:1799–1815
Tynkkynen K, Raatikainen KJ, Häkkilä M, Haukilehto E, Kotiaho JS (2009) Alternative reproductive tactics and the propensity of hybridization. J Evol Biol 22:2512–2518
van Gossum H, Stoks R, De Bruyn L (2001) Reversible frequency-dependent switches in male mate choice. Proc Roy Soc B 268:83–85
Veen T, Borge T, Griffith SC, Saetre GP, Bures S, Gustafsson L, Sheldon BC (2001) Hybridization and adaptive mate choice in flycatchers. Nature 411(6833):45–50
Verzijden MN, Rosenthal GG (2011) Effects of sensory modality on learned mate preferences in female swordtails. Anim Behav 82:557–562
Verzijden MN, ten Cate C (2007) Early learning influences species assortative mating preferences in Lake Victoria cichlid fish. Biol Lett 3:134–136
Verzijden MN, Culumber ZW, Rosenthal GG (2012) Opposite effects of learning cause asymmetric mate preferences in hybridizing species. Behav Ecol 23:1133–1139
West-Eberhard MJ (1983) Sexual selection, social competition and speciation. Q Rev Biol 58:155–183
Wiley C, Fogelberg N, Sæther SA, Veen T, Svedin N, Kehlenbeck JV, Qvarnström A (2007) Direct benefits and costs for hybridizing Ficedula flycatchers. J Evol Biol 20:854–864
Willis PM, Ryan MJ, Rosenthal GG (2011) Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish. Behav Ecol 22:1234–1240
Willis PM, Rosenthal GG, Ryan MJ (2012) An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni. PLoS One 7:e34802
Wilson DS, Hedrick A (1982) Speciation and the economics of mate choice. Evol Theory 6:15–24
Wilson AC, Maxson LR, Sarich VM (1974) Two types of molecular evolution: evidence from studies of interspecific hybridization. Proc Natl Acad Sci USA 71:2843–2847
Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12
Wyman MT, Charlton BD, Locatelli Y, Reby D (2011) Variability of female responses to conspecific vs. heterospecific male mating calls in polygynous deer: an open door to hybridization? PLoS One 6:e23296
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This article benefited from many useful discussions with Michael Ryan, Gil Rosenthal, Michael Singer, Ulrich Mueller, and Dan Bolnick. I thank the two anonymous reviewers for their many helpful comments and suggestions.
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Willis, P.M. Why do animals hybridize?. acta ethol 16, 127–134 (2013). https://doi.org/10.1007/s10211-013-0144-6
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DOI: https://doi.org/10.1007/s10211-013-0144-6