Fertilisation and early developmental barriers to hybridisation in field crickets

BMC Evolutionary Biology

Tom Tregenza¹  Rolando Rodríguez-Muñoz¹  Frances Tyler¹ 

[1] Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Penryn, Cornwall, UK

关键词: Polymorphism;    Variable reproductive isolation;    Gryllus;    Embryogenesis;    Fertilisation;    Hybrid;    Reproductive isolation;    Speciation;   

Others  :  1129791
DOI  :  10.1186/1471-2148-13-43

 received in 2012-10-29, accepted in 2013-02-11,  发布年份 2013

【 摘 要 】

Background

Post-mating interactions between the reproductive traits and gametes of mating individuals and among their genes within zygotes are invariably complex, providing multiple opportunities for reproduction to go awry. These interactions have the potential to act as barriers to gene flow between species, and may be important in the process of speciation. There are multiple post-mating barriers to interbreeding between the hybridising field crickets Gryllus bimaculatus and G. campestris. Female G. bimaculatus preferentially store sperm from conspecific males when mated to both conspecific and heterospecific partners. Additionally, conspecific males sire an even greater proportion of offspring than would be predicted from their sperm’s representation in the spermatheca. The nature of these post-sperm-storage barriers to hybridisation are unknown. We use a fluorescent staining technique to determine whether barriers occur prior to, or during embryo development.

Results

We show that eggs laid by G. bimaculatus females mated to G. campestris males are less likely to begin embryogenesis than eggs from conspecific mating pairs. Of the eggs that are successfully fertilised and start to develop, those from heterospecific mating pairs are more likely to arrest early, prior to blastoderm formation. We find evidence for bimodal variation among egg clutches in the number of developing embryos that subsequently arrest, indicating that there is genetic variation for incompatibility between mating individuals. In contrast to the pattern of early embryonic mortality, those hybrids reaching advanced stages of embryogenesis have survival rates equal to that of embryos from conspecific mating pairs.

Conclusions

Post-sperm-storage barriers to hybridisation show evidence of genetic polymorphism. They are sufficiently large, that if the species interbreed where they are sympatric, these barriers could play a role in the maintenance of reproductive isolation between them. The number of eggs that fail to develop represents a substantial cost of hybridization to G. bimaculatus females, and this cost could reinforce the evolution of barriers occurring earlier in the reproductive process.

【 授权许可】

   
2013 Tyler et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Mayr E: Animal species and evolution. Cambridge, MA: Belknap Press; 1963.
• [2]Mayr E: The biological meaning of species. Biol J Linn Soc 1969, 1(3):311-320.
• [3]Dobzhansky T: Genetics and the Origin of Species. New York: Columbia University Press; 1937.
• [4]Matute DR, Coyne JA: Intrinsic reproductive isolation between two sister species of Drosophila. Evolution 2010, 64(4):903-920.
• [5]Sagga N, Civetta A: Male–female interactions and the evolution of postmating prezygotic reproductive isolation among species of the Virilis subgroup. Int J Evol Biol 2011, 2011:1-11.
• [6]Larson EL, Hume GL, Andrés JA, Harrison RG: Post-mating prezygotic barriers to gene exchange between hybridizing field crickets. J Evol Biol 2012, 25(1):174-186.
• [7]Price CSC, Kim CH, Gronlund CJ, Coyne JA: Cryptic reproductive isolation in the Drosophila Simulans species complex. Evolution 2001, 55(1):81-92.
• [8]Katakura H: Evidence for the incapacitation of heterospecific sperm in the female genital tract in a pair of closely related ladybirds (Insecta, Coleoptera, Coccinellidae). Zoolog Sci 1986, 3:151-121.
• [9]Gregory PG, Howard DJ: A postinsemination barrier to fertilization isolates two closely related ground crickets. Evolution 1994, 48(3):705-710.
• [10]Palumbi SR: Species formation and the evolution of gamete recognition loci. In Endless forms: Species and Speciation. Edited by Howard DJ, Berlocher SH. New York: Oxford University Press; 1998:271-278.
• [11]Coyne JA, Orr HA: Speciation. Sunderland: Sinauer; 2004.
• [12]Kinsey JD: Studies on an embryonic lethal hybrid in Drosophila. J Embryol Exp Morphol 1967, 17(2):405-423.
• [13]Álvarez D, Garcia-Vazquez E: Maintenance of asymmetric hybridization between Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) via postzygotic barriers and paternal effects. Can J Fish Aquat Sci 2011, 68:593-602.
• [14]Sellier N, Brun J-M, Richard M-M, Batellier F, Dupuy V, Brillard J-P: Comparison of fertility and embryo mortality following artificial insemination of common duck females (Anas platyrhynchos) with semen from common or Muscovy (Cairina moschata) drakes. Theriogenology 2005, 64(2):429-439.
• [15]Huang Y, Ortí G, Sutherlin M, Duhachek A, Zera A: Phylogenetic relationships of North American field crickets inferred from mitochondrial DNA data. Mol Phylogenet Evol 2000, 17(1):48-57.
• [16]Pardo JE, Gomes R, Del Cerro A: Orthopteroidea from the mountain chains of Castilla-La Mancha (Spain). II. Ensifera. Zoologica Baetica 1993, 4:113-148.
• [17]Gorochov AV, Llorente V: Estudio taxonómico preliminar de los Grylloidea de España (Insecta, Orthoptera). Graellsia 2001, 57(2):95-139.
• [18]Popov AV, Shuvalov VF: Phonotactic behavior of crickets. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 1977, 119(1):111-126.
• [19]Veen T, Faulks J, Rodríguez-Muñoz R, Tregenza T: Premating reproductive barriers between hybridising cricket species differing in their degree of polyandry. PLoS One 2011, 6(5):e19531.
• [20]von Hörmann-Heck S: Untersuchungen über den Erbgang eininger Verhaltensweisen bei Grillenbastarden. Zeitschrift Fur Tierpsychologie 1957, 14:137-183.
• [21]Tyler F, Harrison X, Bretman A, Veen T, Rodríguez-Muñoz R, Tregenza T: Multiple post-mating barriers to hybridisation in field crickets. Mol Ecol 2013.
• [22]Simmons LW: Female choice in the field cricket Gryllus bimaculatus (De Geer). Anim Behav 1986, 34(5):1463-1470.
• [23]Walker WF: Sperm utilization strategies in nonsocial insects. Am Nat 1980, 115(6):780-799.
• [24]Parker GA: Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 1982, 96:281-294.
• [25]O'Rand MG: Sperm-egg recognition and barriers to interspecies fertilization. Gamete Res 1988, 19(4):315-327.
• [26]Alipaz JA, Wu C, Karr TL: Gametic incompatibilities between races of Drosophila melanogaster. Proc R Soc Lond B Biol Sci 2001, 268(1469):789-795.
• [27]Manier MK, Belote JM, Berben KS, Novikov D, Stuart WT, Pitnick S: Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 2010, 328(5976):354-357.
• [28]Cutter AD: The polymorphic prelude to Bateson–Dobzhansky–Muller incompatibilities. Trends Ecol Evol 2012, 27(4):209-218.
• [29]Bateson W: Heredity and variation in modern lights. Cambridge: Cambridge University Press; 1909:85-101. [Darwin and Modern Science]
• [30]Dobzhansky T: Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 1936, 21:113-135.
• [31]Muller H: Isolating mechanisms, evolution and temperature. Biol Symp 1942, 6:71-125.
• [32]Lemmon EM, Lemmon AR: Reinforcement in chorus frogs: Lifetime fitness estimates including intrisnsic natural selection and sexual selection against hybrids. Evolution 2010, 64(6):1748-1761.
• [33]López-Fernández H, Bolnick DI: What causes partial F1 hybrid viability? Incomplete penetrance versus genetic variation. PLoS One 2007, 2(12):e1294.
• [34]Shuker DM, Underwood K, King TM, Butlin RK: Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proceedings of the Royal Society B: Biological Sciences 2005, 272(1580):2491-2497.
• [35]Reed LK, Markow TA: Early events in speciation: Polymorphism for hybrid male sterility in Drosophila. Proc Natl Acad Sci USA 2004, 101(24):9009-9012.
• [36]Good JM, Handel MA, Nachman MW: Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 2008, 62(1):50-65.
• [37]Sarashina I, Mito T, Saito M, Uneme H, Miyawaki K, Shinmyo Y, Ohuchi H, Noji S: Location of micropyles and early embryonic development of the two-spotted cricket Gryllus bimaculatus (Insecta, Orthoptera). Dev Growth Differ 2005, 47(2):99-108.
• [38]Kaufmann BP: The nature of hybrid sterility - abnormal development in eggs of hybrids between Drosophila miranda and Drosophila pseudoobscura. J Morphol 1940, 66(2):197-213.
• [39]Mitrofanov VG, Sidorova NV: Genetics of the sex ratio anomaly in Drosophila hybrids of the Virilis group. Theor Appl Genet 1981, 59(1):17-22.
• [40]Raff EC, Popodi EM, Sly BJ, Turner FR, Villinski JT, Raff RA: A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 1999, 126(9):1937-1945.
• [41]Baird SE, Yen W-C: Reproductive isolation in Caenorhabditis: terminal phenotypes of hybrid embryos. Evol Dev 2000, 2(1):9-15.
• [42]Elinson RP: Genetic analysis of developmental arrest in an amphibian hybrid (Rana catesbeiana, Rana clamitans). Dev Biol 1981, 81(1):167-176.
• [43]Volpe EP: Intensity of reproductive isolation between sympatric and allopatric populations of Bufo americanus and Bufo fowleri. Am Nat 1955, 89(848):303-317.
• [44]Barton NH, Hewitt GM: The genetic basis of hybrid inviability in the grasshopper Podisma pedestris. Heredity 1981, 47(3):367-383.
• [45]Piavis GW, Howell JH, Smith AJ: Experimental hybridization among five species of lampreys from the Great Lakes. Copeia 1970, 1970(1):29-37.
• [46]Wu C-I, Davis AW: Evolution of postmating reproductive isolation: The composite nature of Haldane's rule and its genetic bases. Am Nat 1993, 142(2):187-212.
• [47]True JR, Weir BS, Laurie CC: A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 1996, 142(3):819-837.
• [48]Turelli M, Orr HA: Dominance, Epistasis and the Genetics of Postzygotic Isolation. Genetics 2000, 154(4):1663-1679.
• [49]Noor MAF, Grams KL, Bertucci LA, Reiland J: Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci 2001, 98(21):12084-12088.
• [50]Cousin G: Sur l'hybridation de deux espèces de Gryllidae (Acheta campestris et bimaculata). Bulletin de la Socièté entomologique de France 1933, 12:189-193.
• [51]Sato M, Tanaka-Sato H: Fertilization, syngamy, and early embryonic development in the cricket Gryllus bimaculatus (de geer). J Morphol 2002, 254(3):266-271.
• [52]Sarashina I, Shinmyo Y, Hirose A, Miyawaki K, Mito T, Ohuchi H, Horio T, Noji S: Hypotonic buffer induces meiosis and formation of anucleate cytoplasmic islands in the egg of the two-spotted cricket Gryllus bimaculatus. Dev Growth Differ 2003, 45(2):103-112.
• [53]Bates D, Maechler M, Bolker B: lme4: Linear mixed-effects models using S4 classes. 2011. R package version 0.999375-28. edn
• [54]Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2011.
• [55]Crawley MJ: The R Book. Chichester: Wiley; 2007.