Barriers to gene exchange in hybridizing field crickets: the role of male courtship effort and cuticular hydrocarbons

BMC Evolutionary Biology

David P Richardson³  Erica L Larson²  Joy Jing⁴  Elizabeth Hart¹  Zachary M McKenzie¹  Luana S Maroja¹ 

[1] Department of Biology, Williams College, 31 Morley Drive, 01267 Williamstown, MA, USA;Division of Biological Sciences, University of Montana, 59802 Missoula, MT, USA;Department of Chemistry, Williams College, 01267 Williamstown, MA, USA;Department of Mathematics and Statistics, Williams College, 01267 Williamstown, MA, USA

关键词: Pheromone;    Pre-zygotic;    Barrier to gene exchange;    Behavior;    Gryllus pennsylvanicus;    Gryllus firmus;   

Others  :  857534
DOI  :  10.1186/1471-2148-14-65

 received in 2014-03-06, accepted in 2014-03-17,  发布年份 2014

【 摘 要 】

Background

Pre-zygotic barriers often involve some form of sexual selection, usually interpreted as female choice, as females are typically the choosier sex. However, males typically show some mate preferences, which are increasingly reported. Here we document previously uncharacterized male courtship behavior (effort and song) and cuticular hydrocarbon (CHC) profiles in the hybridizing crickets Gryllus firmus and G. pennsylvanicus. These two species exhibit multiple barriers to gene exchange that act throughout their life history, including a behavioral barrier that results in increased time to mate in heterospecific pairs.

Results

We demonstrated that male mate choice (as courtship effort allocation) plays a more important role in the prezygotic behavioral barrier than previously recognized. In gryllids females ultimately decide whether or not to mate, yet we found males were selective by regulating courtship effort intensity toward the preferred (conspecific) females. Females were also selective by mating with more intensely courting males, which happened to be conspecifics. We report no differences in courtship song between the two species and suggest that the mechanism that allows males to act differentially towards conspecific and heterospecific females is the cuticular hydrocarbon (CHC) composition. CHC profiles differed between males and females of both species, and there were clear differences in CHC composition between female G. firmus and G. pennsylvanicus but not between the males of each species.

Conclusion

Although many barriers to gene exchange are known in this system, the mechanism behind the mate recognition leading to reduced heterospecific mating remains unknown. The CHC profiles might be the phenotypic cue that allow males to identify conspecifics and thus to adjust their courtship intensity accordingly, leading to differential mating between species.

【 授权许可】

   
2014 Maroja et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Coyne JA, Orr HA: Speciation. Sunderland, Mass: Sinauer Associates, Inc. Publishers; 2004.
• [2]Andersson MB: Sexual Selection. Princeton, N.J.: Princeton University Press; 1994.
• [3]Edward DA, Chapman T: The evolution and significance of male mate choice. Trends Ecol Evol 2011, 26(12):647-654.
• [4]Amundsen T, Forsgren E: Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci U S A 2001, 98(23):13155-13160.
• [5]Bel-Venner MC, Dray S, Allaine D, Menu F, Venner S: Unexpected male choosiness for mates in a spider. Proc R Soc B-Biol Sci 2008, 275(1630):77-82.
• [6]Reading KL, Backwell PRY: Can beggars be choosers? Male mate choice in a fiddler crab. Anim Behav 2007, 74:867-872.
• [7]Kokko H, Monaghan P: Predicting the direction of sexual selection. Ecol Lett 2001, 4(2):159-165.
• [8]Kokko H, Johnstone RA: Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc Lond B Biol Sci 2002, 357(1419):319-330.
• [9]Servedio MR, Lande R: Population genetic models of male and mutual mate choice. Evolution 2006, 60(4):674-685.
• [10]South SH, Arnqvist G, Servedio MR: Female preference for male courtship effort can drive the evolution of male mate choice. Evolution 2012, 66(12):3722-3735.
• [11]Scudder SH: The species of Gryllus found in the United States east of Sierra Nevadas. Psyche 1902, 9(309):294-295.
• [13]Harrison RG, Arnold J: A narrow hybrid zone between closely related cricket species. Evolution 1982, 36(3):535-552.
• [14]Harrison RG, Bogdanowicz SM: Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution 1997, 51(2):493-505.
• [15]Maroja LS, Andres JA, Harrison RG: Genealogical discordance and patterns of introgression and selection across a cricket hybrid zone. Evolution 2009, 63(11):2999-3015.
• [16]Larson EL, Becker CG, Bondra ER, Harrison RG: Structure of a mosaic hybrid zone between the field crickets Gryllus firmus and G. pennsylvanicus. Ecology and Evolution 2013, 3(4):985-1002.
• [17]Harrison RG: Barriers to gene exchange between closely related cricket species.1. Laboratory hybridization studies. Evolution 1983, 37(2):245-251.
• [18]Harrison RG: Barriers to gene exchange between closely related cricket species.2. Life-cycle variation and temporal isolation. Evolution 1985, 39(2):244-259.
• [19]Ross CL, Harrison RG: A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution 2002, 56(11):2296-2312.
• [20]Ross CL, Harrison RG: Viability selection on overwintering eggs in a field cricket mosaic hybrid zone. Oikos 2006, 115(1):53-68.
• [21]Larson EL, Hume GL, Andres JA, Harrison RG: Post-mating prezygotic barriers to gene exchange between hybridizing field crickets. J Evol Biol 2012, 25(1):174-186.
• [22]Maroja LS, Andres JA, Walters JR, Harrison RG: Multiple barriers to gene exchange in a field cricket hybrid zone. Biol J Linn Soc 2009, 97(2):390-402.
• [23]Mendelson TC, Shaw KL: The (mis)concept of species recognition. Trends Ecol Evol 2012, 27(8):421-427.
• [24]Etges WJ, Ahrens MA: Premating isolation is determined by larval-rearing substrates in cactophilic Drosophila mojavensis. V. Deep geographic variation in epicuticular hydrocarbons among isolated populations. Am Nat 2001, 158(6):585-598.
• [25]Etges WJ, de Oliveira CC, Ritchie MG, Noor MAF: Genetics of incipient speciation in drosophila mojavensis: Ii. Host plants and mating status influence cuticular hydrocarbon Qtl expression and G X E interactions. Evolution 2009, 63(7):1712-1730.
• [26]Howard RW, Mcdaniel CA, Nelson DR, Blomquist GJ, Gelbaum LT, Zalkow LH: Cuticular hydrocarbons of reticulitermes virginicus (banks) (isoptera, rhinotermitidae) and their role as potential species-recognition and caste-recognition cues. J Chem Ecol 1982, 8(9):1227-1239.
• [27]Howard RW, Blomquist GJ: Ecological, behavioral, andbiochemical aspects of insect hydrocarbons. Annu Rev Entomol 2005, 50:371-393.
• [28]Peterson MA, Dobler S, Larson EL, Juarez D, Schlarbaum T, Monsen KJ, Francke W: Profiles of cuticular hydrocarbons mediate male mate choice and sexual isolation between hybridising Chrysochus (Coleoptera: Chrysomelidae). Chemoecology 2007, 17(2):87-96.
• [29]Buellesbach J, Gadau J, Beukeboom LW, Echinger F, Raychoudhury R, Werren JH, Schmitt T: Cuticular hydrocarbon divergence in the jewel wasp Nasonia: evolutionary shifts in chemical communication channels? J Evol Biol 2013, 26(11):2467-2478.
• [30]Havens JA, Etges WJ: Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IX. Host plant and population specific epicuticular hydrocarbon expression influences mate choice and sexual selection. J Evol Biol 2013, 26(3):562-576.
• [31]Mullen SP, Mendelson TC, Schal C, Shaw KL: Rapid evolution of cuticular hydrocarbons in a species radiation of acoustically diverse Hawaiian crickets (Gryllidae: Trigonidiinae: Laupala). Evolution 2007, 61(1):223-231.
• [32]Nagamoto J, Aonuma H, Hisada M: Discrimination of conspecific individuals via cuticular pheromones by males of the cricket Gryllus bimaculatus. Zool Sci 2005, 22(10):1079-1088.
• [33]Thomas ML, Simmons LW: Sexual dimorphism in cuticular hydrocarbons of the Australian field cricket Teleogryllus oceanicus (Orthoptera: Gryllidae). J Insect Physiol 2008, 54(6):1081-1089.
• [34]R Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013. http://www.R-project.org/ webcite
• [35]Crawley MJ: The R book. Chichester, England: Hoboken, N.J.: Wiley; 2007.
• [36]Ming QL, Lewis SM: Mate recognition and sex differences in cuticular hydrocarbons of the diurnal firefly Ellychnia corrusca (Coleoptera: Lampyridae). Ann Entomol Soc Am 2010, 103(1):128-133.
• [37]Oksanen J, Blanchet FG, Kindt R, Legendre P, Solymos M, Stevens HH, Wagner H, Minchin PROHRB, G.L. S, P: Vegan: community ecology package. 2013. R package version 20–8, http://CRAN.R-project.org/package=vegan
• [38]Williams H, Mehta N: Changes in adult zebra pinch song require a forebrain nucleus that is not necessary for song production. J Neurobiol 1999, 39(1):14-28.
• [39]Oh KP, Fergus DJ, Grace JL, Shaw KL: Interspecific genetics of speciation phenotypes: song and preference coevolution in Hawaiian crickets. J Evol Biol 2012, 25(8):1500-1512.
• [40]Byers J, Hebets E, Podos J: Female mate choice based upon male motor performance. Anim Behav 2010, 79(4):771-778.
• [41]Adamo SA, Hoy RR: Mating behaviour of the field cricket Gryllus bimaculatus and its dependence on social and environmental cues. Anim Behav 1994, 47(4):857-868.
• [42]Hissmann K: Strategies of mate finding in the European field cricket (Gryllus campestris) at different population densities: a field study. Ecological Entomology 1990, 15(3):281-291.
• [43]Saleh N, Larson E, Harrison R: Reproductive success and body size in the cricket Gryllus firmus. J Insect Behav 2013, 1-11. doi:10.1007/s10905-013-9425-1
• [44]Groning J, Hochkirch A: Reproductive interference between animal species. Q Rev Biol 2008, 83(3):257-282.
• [45]Hochkirch A, Lemke I: Asymmetric mate choice, hybridization, and hybrid fitness in two sympatric grasshopper species. Behav Ecol Sociobiol 2011, 65(8):1637-1645.
• [46]Clutton-Brock T, Langley P: Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Behav Ecol 1997, 8(4):392-395.
• [47]Cordts R, Partridge L: Courtship reduces longevity of male Drosophila melanogaster. Anim Behav 1996, 52(2):269-278.
• [48]Mappes J, Alatalo RV, Kotiaho J, Parri S: Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc R Soc Lond Ser B Biol Sci 1996, 263(1371):785-789.
• [49]Pomiankowski A: Sexual selection - the handicap principle does work sometimes. Proc R Soc Ser B-Bio 1987, 231(1262):123-145.
• [50]Johnstone RA: Sexual selection, honest advertisement and the handicap principle - reviewing the evidence. Biol Rev Camb Philos Soc 1995, 70(1):1-65.
• [51]Burk T: Male Aggression and Female Choice in a Field Cricket (Teleogryllus Oceanicus): the Importance of Courtship Song. In Orthopteran Mating Systems - Sexual Competition in a Diverse Group of Insects. Edited by Gwynne DT, Morris GK. : Boulder: Westview Press; 1983:97-119.
• [52]Libersat F, Murray JA, Hoy RR: Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis. J Comp Physiol A 1994, 174(4):485-494.
• [53]Nelson CM, Nolen TG: Courtship song, male agonistic encounters, and female mate choice in the house cricket, Acheta domesticus (Orthoptera: Gryllidae). J Insect Behav 1997, 10(4):557-570.
• [54]Rebar D, Bailey NW, Zuk M: Courtship song’s role during female mate choice in the field cricket Teleogryllus oceanicus. Behav Ecol 2009, 20(6):1307-1314.
• [55]Thomas ML, Simmons LW: Male crickets adjust the viability of their sperm in response to female mating status. Am Nat 2007, 170(2):190-195.
• [56]Ruiz M, Beals ZM, Martins EP: Male sagebrush lizards (sceloporus graciosus) increase exploratory behavior toward females with more courtship experience. Herpetologica 2010, 66(2):142-147.
• [57]Roberts JA, Uetz GW: Information content of female chemical signals in the wolf spider, Schizocosa ocreata: male discrimination of reproductive state and receptivity. Anim Behav 2005, 70:217-223.
• [58]Lihoreau M, Zimmer C, Rivault C: Mutual mate choice: when it pays both sexes to avoid inbreeding. Plos One 2008, 3(10):e3365. 3361–3367
• [59]Herdman EJE, Kelly CD, Godin J-GJ: Male mate choice in the guppy (Poecilia reticulata): do males prefer larger females as mates? Ethology 2004, 110(2):97-111.
• [60]Doherty JA, Storz MM: Calling song and selective phonotaxis in the field crickets, Gryllus firmus and G. pennsylvanicus (Orthoptera: Gryllidae). J Insect Behav 1992, 5(5):555-569.
• [61]Alexander RD: Life cycle origins, speciation, and related phenomena in crickets. Q Rev Biol 1968, 43:1-41.
• [62]Fitzpatrick MJ, Gray DA: Divergence between the courtship songs of the field crickets Gryllus texensis and Gryllus rubens (Orthoptera, Gryllidae). Ethology 2001, 107(12):1075-1085.
• [63]Grace JL, Shaw KL: Coevolution of male mating signal and female preference during early lineage divergence of the hawaiian cricket, Laupala Cerasina. Evolution 2011, 65(8):2184-2196.
• [64]Zuk M, Simmons LW: Reproductive Strategies of the Crickets (Orthoptera: Gryllidae). In The Evolution of Mating Systems in Insects and Arachnids. Edited by Choe JC, Crespi BJ. Cambridge, New York & Melbourne: Cambridge University Press; 1997:89-109.
• [65]Gray DA, Cade WH: Sexual selection and speciation in field crickets. Proc Natl Acad Sci U S A 2000, 97(26):14449-14454.
• [66]Honda-Sumi E: Difference in calling song of three field crickets of the genus Teleogryllus: the role in premating isolation. Anim Behav 2005, 69(4):881-889.
• [67]Balakrishnan R, Pollack GS: Recognition of courtship song in the field cricket, Teleogryllus oceanicus. Anim Behav 1996, 51(2):353-366.
• [68]Zuk M, Rebar D, Scott SP: Courtship song is more variable than calling song in the field cricket Teleogryllus oceanicus. Anim Behav 2008, 76:1065-1071.
• [69]Bailey NW, McNabb JR, Zuk M: Preexisting behavior facilitated the loss of a sexual signal in the field cricket Teleogryllus oceanicus. Behav Ecol 2008, 19(1):202-207.
• [70]Dambach M: Vibrational Responses. In Cricket Behavior and Neurobiology. Edited by Huber F, Moore TE, Loher W. Ithaca: Cornell University Press; 1989:178-197.
• [71]Tregenza T, Wedell N: Definitive evidence for cuticular pheromones in a cricket. Anim Behav 1997, 54:979-984.
• [72]Thomas ML, Simmons LW: Crickets detect the genetic similarity of mating partners via cuticular hydrocarbons. J Evol Biol 2011, 24(8):1793-1800.
• [73]Bailey NW: Mate choice plasticity in the field cricket Teleogryllus oceanicus: effects of social experience in multiple modalities. Behav Ecol Sociobiol 2011, 65(12):2269-2278.
• [74]Chenoweth SF, Blows MW: Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata. Am Nat 2005, 165(2):281-289.
• [75]Arnqvist G, Rowe L: Sexual Conflict. Princeton, N.J.: Princeton University Press; 2005.
• [76]Gosden TP, Svensson EI: Density-dependent male mating harassment, female resistance, and male mimicry. Am Nat 2009, 173(6):709-721.
• [77]Svensson EI, Abbott JK, Gosden TP, Coreau A: Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evol Ecol 2009, 23(1):93-108.
• [78]Cordoba-Aguilar A: Dragonflies and Damselflies: Model Organisms for Ecological and Evolutionary Research. Oxford: New York: Oxford University Press; 2008.
• [79]Bots J, De Bruyn L, Van Dongen S, Smolders R, Van Gossum H: Female polymorphism, condition differences, and variation in male harassment and ambient temperature. Biol J Linn Soc 2009, 97(3):545-554.
• [80]Gay L, Eady PE, Vasudev R, Hosken DJ, Tregenza T: Costly sexual harassment in a beetle. Physiol Entomol 2009, 34(1):86-92.
• [81]Bateman PW, Ferguson JWH, Yetman CA: Courtship and copulation, but not ejaculates, reduce the longevity of female field crickets (Gryllus bimaculatus). J Zool 2006, 268(4):341-346.
• [82]Simmons LW: Sexual selection and body size in a natural population of field cricket, Gryllus campestris (L.). J Orthoptera Res 1992, 1:12-13.
• [83]Bateman PW: Burrow residency, access to females and body size in male Scapsipedus meridianus Otte & Cade (Orthoptera: Gryllidae; Gryllinae). J Orthoptera Res 2000, 9:27-29.
• [84]Sakaluk SK: Post-copulatory mate guarding in decorated crickets. Anim Behav 1991, 41(2):207-216.
• [85]Bateman PW, MacFadyen DN: Mate guarding in the cricket Gryllodes sigillatus: influence of multiple potential partners. Ethology 1999, 105(11):949-957.
• [86]Bussiere LF, Hunt J, Jennions MD, Brooks R: Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus. Evolution 2006, 60(4):792-800.
• [87]Fincke OM: Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 2004, 67(5):833-845.
• [88]Gavrilets S, Waxman D: Sympatric speciation by sexual conflict. Proc Natl Acad Sci U S A 2002, 99(16):10533-10538.