Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

Journal of Evolutionary Biology

Volumn 27, Issue 9, 2014, Pages 1811-1818

  Vasudeva, R ^a   Deeming, D C ^a   Eady, P E ^a  

^a UNIVERSITY OF LINCOLN   (United Kingdom)

Author keywords

Ontogeny; Phenotypic plasticity; Primary reproductive traits; Reaction norm; Sexual selection

Indexed keywords

BEETLE; BODY SIZE; DEVELOPMENTAL STAGE; FITNESS; LIFE HISTORY TRAIT; ONTOGENY; PHENOTYPIC PLASTICITY; REACTION NORM; REPRODUCTIVE BIOLOGY; SEXUAL SELECTION; SPERM COMPETITION; TEMPERATURE EFFECT;

BRUCHINAE; CALLOSOBRUCHUS MACULATUS; COLEOPTERA;

EID: 84901384861     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12431     Document Type: Article

References (63)

1. Abramoff, M.D., Magalhaes, P.J. & Ram, S.J. 2004. Image processing with ImageJ. Biophotonics Int. 11: 36-42.
2. Amitin, E.G. & Pitnick, S. 2006. Influence of developmental environment on male and female mediated sperm precedence in Drosophila melanogaster. J. Evol. Biol. 20: 381-391.
3. Angilletta, M.J. Jr, Wilson, R.S., Navas, C.A. & James, R.S. 2003. Tradeoffs and the evolution of thermal reaction norms. Trends Ecol. Evol. 18: 234-240.
4. Appleby, J.H. & Credland, P.F. 2007. The role of temperature and larval crowding in morph determination in a tropical beetle, Callosobruchus maculatus. J. Insect Physiol. 53: 983-993.
5. Atkinson, D. 1994. Temperature and organism size: a biological law for ectotherms? Adv. Ecol. Res. 25: 1-58.
6. Berger, D., Bauerfeind, S.S., Blanckenhorn, W.U. & Schäfer, M.A. 2011. High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution 65: 2830-2842.
7. Bergmann, C. 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Studien 3: 595-708.
8. Birkhead, T.R. & Møller, A.P. 1998. Sperm Competition and Sexual Selection. Academic Press, London.
9. Bjork, A., Starmer, W.T., Higginson, D.M., Rhodes, C.J. & Pitnick, S. 2007. Complex interactions with females and rival males limit the evolution of sperm offence and sperm defence. Proc. R. Soc. Lond. B 274: 1779-1788.
10. Blanckenhorn, W.U. & Hellriegel, B. 2002. Against Bergmann's rule: fly sperm size increases with temperature. Ecol. Lett. 5: 7-10.
11. Breckels, R.D. & Neff, D.D. 2013. The effects of elevated temperature on the sexual traits, immunology and survivorship of a tropical ectotherm. J. Exp. Biol. 216: 2658-2664.
12. Brown, D.V. & Eady, P.E. 2001. Functional incompatibility between the fertilization systems of two allopatric populations of Callosobruchus maculatus (Coleoptera: Bruchidae). Evolution 55: 2257-2262.
13. Burke, T. 1989. DNA fingerprinting and other methods for the study of mating success. Trends Ecol. Evol. 4: 139-144.
14. Calhim, S., Immler, S. & Birkhead, T.R. 2007. Postcopulatory sexual selection decreases variation in sperm morphology. PLoS One 2: e413.
15. Crawley, M.J. 2002. Statistical Computing: An Introduction to Data Analysis Using S-PLUS. John Wiley & Sons, Chichester.
16. Crean, A.J. & Marshall, D.J. 2008. Gamete plasticity in a broadcast spawning marine invertebrate. Proc. Natl. Acad. Sci. USA 105: 13508-13513.
17. Devereau, A.D., Gudrups, I., Appleby, J.H. & Credland, P.F. 2003. Automatic, rapid screening of seed resistance in cowpea, Vigna unguiculata (L.) Walpers, to the seed beetle Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) using acoustic monitoring. J. Stored Prod. Res. 39: 117-129.
18. Eady, P.E. 1991. Sperm competition in Callosobruchus maculatus (Coleoptera: Bruchidae): a comparison of two methods used to estimate paternity. Ecol. Entomol. 16: 45-53.
19. Eady, P.E. 1994. Intraspecific variation in sperm precedence in Callosobruchus maculatus. Ecol. Entomol. 16: 45-53.
20. Eady, P.E. 1995. Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav. Ecol. Sociobiol. 36: 25-32.
21. Eady, P.E., Wilson, N. & Jackson, M. 2000. Copulating with multiple mates enhances female fecundity but not egg-to-adult survival in the bruchid beetle Callosobruchus maculatus. Evolution 54: 2161-2165.
22. Eberhard, W.G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, Princeton, NJ.
23. Espinosa-Soto, C., Martin, O.C. & Wagner, A. 2011. Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol. Biol. 11: 1-14.
24. Fitzpatrick, J.L. & Baer, B. 2011. Polyandry reduces sperm length variation in social insects. Evolution 65: 3006-3012.
25. Fox, C.W., Hickman, D.L., Raleigh, E.L. & Mousseau, T.A. 1995. Paternal investment in a seed beetle (Coleoptera: Bruchidae): influence of male size, age, and mating history. Ann. Ent. Soc. Am. 88: 100-103.
26. Fox, C.W., Stillwell, R.C., Wallin, W.G. & Hitchcock, L.J. 2006. Temperature and host species affect nuptial gift size in a seed-feeding beetle. Funct. Ecol. 20: 1003-1011.
27. Gage, M.J.G. 1991. Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit fly. Anim. Behav. 42: 1036-1047.
28. Gage, M.J.G. & Cook, P.A. 1994. Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in moth Plodia interpunctella (Lepidoptera: Pyralidae). Funct. Ecol. 8: 594-599.
29. Gay, L., Hosken, D.J., Vasudev, R., Tregenza, T. & Eady, P.E. 2009. Sperm competition and maternal effects differentially influence testis and sperm size in Callosobruchus maculatus. J. Evol. Biol. 22: 1143-1150.
30. Gomez-Mestre, I. & Jovani, R. 2013. A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation. Proc. R. Soc. B 280: 20131869.
31. Hellriegel, B. & Blanckenhorn, W.U. 2002. Environmental influences on the gametic investment of yellow dung fly males. Evol. Ecol. 16: 505-522.
32. Immler, S., Calhim, S. & Birkhead, T.R. 2008. Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62: 1538-1543.
33. Kelly, C.D. & Jennions, M.D. 2011. Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol. Rev. 86: 863-884.
34. Kvarnemo, C. & Simmons, L.W. 2013. Polyandry as a mediator of sexual selection before and after mating. Philos. Trans. R. Soc. B 368: 20120042.
35. Kvist, J., Wheat, C.W., Kallioniemi, E., Saastamoinen, M., Hanski, I. & Frilander, M.J. 2013. Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol. Ecol. 22: 602-619.
36. Lande, R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22: 1435-1446.
37. van Lieshout, E., Tomkins, J.L. & Simmons, L.W. 2013. Heat stress but not inbreeding affects offensive sperm competitiveness in Callosobruchus maculatus. Ecol. Evol. 3: 2859-2866.
38. Miller, G.T. & Pitnick, S. 2002. Sperm-female coevolution in Drosophila. Science 298: 1230-1233.
39. Minoretti, N., Stoll, P. & Baur, B. 2013. Heritability of sperm length and adult shell size in the land snail Arianta arbustorum (Linnaeus, 1758). J. Molluscan Stud. 79: 218-224.
40. Morrow, E.H., Leijon, A. & Meerupati, A. 2008. Hemiclonal analysis reveals significant genetic, environmental and genotype x environment effects on sperm size in Drosophila melanogaster. J. Evol. Biol. 21: 1692-1702.
41. Parker, G.A. 1970. Sperm competition and its evolutionary consequences in insects. Biol. Rev. 45: 525-567.
42. Parker, G.A. & Simmons, L.W. 1994. Evolution of phenotypic optima and copula in dungflies. Nature 370: 53-56.
43. Penttilä, A., Slade, E.M., Simojoki, A., Riutta, T., Minkkinen, K. & Roslin, T. 2013. Quantifying beetle-mediated effects on gas fluxes from dung pats. PLoS One 8: e71454.
44. Pfennig, D.W., Wund, M.A., Snell-Rood, E.C., Cruickshank, T., Schlichting, C.D. & Moczek, A.P. 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25: 459-467.
45. Pitnick, S., Spicer, G.S. & Markow, T.A. 1995. How long is a giant sperm? Nature 375: 109.
46. Pitnick, S., Hosken, D.J. & Birkhead, T.R. 2009. Sperm morphological diversity. In: Sperm Biology: An Evolutionary Perspective (T.R. Birkhead, D.J. Hosken & S. Pitnick, eds), pp. 69-149. Academic Press, London.
47. Rugman-Jones, P.F. & Eady, P.E. 2007. Conspecific sperm precedence in Callosobruchus subinnotatus (Coleoptera: Bruchidae): mechanisms and consequences. Proc. R. Soc. B 274: 983-988.
48. Rugman-Jones, P.F. & Eady, P.E. 2008. Co-evolution of male and female reproductive traits across the Bruchidae (Coleoptera). Funct. Ecol. 22: 880-886.
49. Schäfer, M.A., Berger, D., Jochmann, R., Blanckenhorn, W.U. & Brussière, L.F. 2013. The developmental plasticity and functional significance of an additional sperm storage compartment in female yellow dung flies. Funct. Ecol. 27: 1392-1402.
50. Schütt, C. & Nöthiger, R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127: 667-677.
51. Sharma, M.D., Minder, A.M. & Hosken, D.J. 2013. No association between sperm competition and sperm length variation across dung flies (Scathophagidae). J. Evol. Biol. 26: 2341-2349.
52. Sharpe, R.M. 2010. Environmental/lifestyle effects on spermatogenesis. Philos. Trans. R. Soc. Lond. B 365: 1697-1712.
53. Simmons, L.W. 2001. Sperm Competition and Its Evolutionary Consequences in Insects. Princeton University Press, Princeton, NJ.
54. Simmons, L.W. & Kotiaho, J.S. 2002. Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56: 1622-1631.
55. Simmons, L.W. & Kotiaho, J.S. 2007. Quantitative genetic correlation between trait and preference supports sexually selected sperm process. Proc. Natl. Acad. Sci. USA 104: 16604-16608.
56. Smith, R.L. 1984. Sperm Competition and the Evolution of Animal Mating Systems. Academic Press, London.
57. Snook, R.R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20: 46-53.
58. Sultan, S.E. 2007. Development in context: the timely emergence of eco-devo. Trends Ecol. Evol. 22: 575-582.
59. Swanson, W.J. & Vacquier, V.D. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3: 137-144.
60. Valenzuela, N. & Lance, V. 2004. Temperature Dependent Sex Determination in Vertebrates. Smithsonian Books, Washington D.C.
61. Van Dooremalen, C., Koekkoek, J. & Ellers, J. 2011. Temperature-induced plasticity in membrane and storage lipid composition: thermal reaction norms across five different temperatures. J. Insect Physiol. 57: 285-291.
62. Wilson, K. & Hill, L. 1989. Factors affecting egg maturation in the bean weevil Callosobruchus maculatus. Physiol. Entomol. 14: 115-126.
63. Wilson, N., Tubman, S.C., Eady, P.E. & Robertson, G.W. 1997. Female genotype affects male success in sperm competition. Proc. R. Soc. Lond. B 264: 1491-1495.