Evolutionary change in testes tissue composition among experimental populations of house mice

Evolution

Volumn 69, Issue 3, 2015, Pages 848-855

  Firman, Renée C ^a   Garcia Gonzalez, Francisco ^a,b   Thyer, Evan ^a   Wheeler, Samantha ^a   Yamin, Zayaputeri ^a   Yuan, Michael ^a   Simmons, Leigh W ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

Author keywords

Histology; Postcopulatory sexual selection; Sperm competition; Sperm production; Testosterone production

Indexed keywords

EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; HISTOLOGY; HYPOTHESIS TESTING; IMAGE ANALYSIS; MONOGAMY; RODENT; SEXUAL SELECTION; SPERM COMPETITION;

MUS MUSCULUS; MUS MUSCULUS DOMESTICUS;

ANATOMY AND HISTOLOGY; ANIMAL; EVOLUTION; MALE; MOUSE; ORGAN SIZE; SEMINIFEROUS TUBULE; SEXUAL BEHAVIOR; SPERMATOZOON COUNT; TESTIS;

ANIMALS; BIOLOGICAL EVOLUTION; MALE; MICE; ORGAN SIZE; SEMINIFEROUS TUBULES; SEXUAL BEHAVIOR, ANIMAL; SPERM COUNT; TESTIS;

EID: 84924972022     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12603     Document Type: Article

References (67)

1. Almbro, M., and L. W. Simmons . 2014. Sexual selection can remove an experimentally induced mutation load. Evolution 68:295-300.
2. Arbuthnott, D., and H. D. Rundle . 2012. Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster. Evolution 66:2127-2137.
3. Beatty, R. A. 1957. A pilot experiment with heterospermic insemination in the rabbit. J. Genet. 55:325.
4. Becker, W. A. 1984. Manual of quantitative genetics, 4th ed. Academic Enterprises, Pullman, WA.
5. Birkhead, T. R., D. J. Hosken, and S. Pitnick 2009. Sperm biology: an evolutionary perspective. Academic Press, Burlington, MA.
6. Boschetto, C., C. Gasparini, and A. Pilastro . 2011. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65:813-821.
7. Brown, C. R., and M. B. Brown . 2003. Testis size increases with colony size in cliff swallows. Behav. Ecol. 14: 569-575.
8. Byrne, P. G., J. D. Roberts, and L. W. Simmons . 2002. Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol. 15:347-355.
9. Charlesworth, B., and D. Charlesworth . 1999. The genetic basis of inbreeding depression. Genet. Res. 74:329-340.
10. Clermont, Y. 1972. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52:198-236.
11. Dean, M. D., K. G. Ardlie, and M. W. Nachman . 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15:4141-4151.
12. delBarco-Trillo, J., and M. H. Ferkin . 2004. Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males. Nature 431:446-449.
13. Desjardins, C., J. A. Maruniak, and F. H. Bronson . 1973. Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939-941.
14. Dufau, M. 1996. The lutenizing hormone receptor. Pp. 333-350 in A. H. Payne, M. P. Hardy, and L. D. Russell, eds. The Leydig cell. Cache River Press, Vienna, IL.
15. Dzminiski, M. A., J. D. Roberts, M. Beveridge, and L. W. Simmons . 2010. Among population covariation between sperm competition and ejaculate expenditure in frogs. Behav. Ecol. 21:322-328.
16. Firman, R. C. 2014. Female social preference for males that have evolved via monogamy: evidence of a trade-off between pre- and post-copulatory sexually selected traits? Biol. Lett. 10:20140659.
17. Firman, R. C., and L. W. Simmons . 2008. The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J. Evol. Biol. 21:1524-1533.
18. Firman, R. C. 2010. Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64:1245-1256.
19. Firman, R. C. 2011. Experimental evolution of sperm competitiveness in a mammal. BMC Evol. Biol. 11:19.
20. Firman, R. C., L. Y. Cheam, and L. W. Simmons . 2011. Sperm competition does not influence sperm hook morphology in selection lines of house mice. J. Evol. Biol. 24:856-862.
21. Firman, R. C., I. Klemme, and L. W. Simmons . 2013. Strategic adjustments in sperm production within and between two island populations of house mice. Evolution 67:3061-3070.
22. Fuentes, L. B., N. Caravaca, L. E. Pelzer, L. A. Scardapane, R. S. Piezzi, and J. A. Guzman . 1991. Seasonal variations in the testes and epididymis of vizcacha (Lagostomus maximus maximus). Biol. Reprod. 45:493-497.
23. Gage, M. J. G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. Lond. B Biol. Sci. 258:247-254.
24. Gage, M. J. G., and E. H. Morrow . 2003. Experimental evidence of the evolution of numerous, tiny sperm via sperm competition. Curr. Biol. 13:754-757.
25. Gier, H. T., and G. B. Marion . 1970. Development of the mammalian testis. Pp. 1-45 in A. D. Johnson, W. R. Gomes, and N. L. Vandemark, eds. The testis. Academic Press, New York.
26. Goldberg, S. R., and W. S. Parker . 1975. Seasonal testicular histology of the colubrid snakes, Masticophis taeniatus and Pituophis melanoleucus. Herpetologica 31:317-322.
27. Gomendio, M., A. H. Harcourt, and E. R. S. Roldan . 1998. Sperm competition in mammals. Pp. 667-755 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, San Diego.
28. Harcourt, A. H., P. H. Harvey, S. G. Larson, and R. V. Short . 1981. Testis weight, body weight and breeding system in the primates. Nature 293:55-57.
29. Harvey, S., J. Bozena, and M. Novotny . 1989. Pattern of volatile compounds in dominant and subordinate male mouse urine. J. Chem. Ecol. 15:2061-2072.
30. Hochereau-de Reviers, M. H., and G. A. Lincoln . 1978. Seasonal variation in the histology of the testis of the red deer, Cervus elaphus. J. Reprod. Fertil. 54:209-213.
31. Hollis, B., J. L. Fierst, and D. Houle . 2009. Sexual selection accelerates the elimination of a deleterious mutant in Drosophila melanogaster. Evolution 63:324-333.
32. Hosken, D. J. 1997. Sperm competition in bats. Proc. R. Soc. Lond. B Biol. Sci. 264:385-392.
33. Hosken, D. J., and P. I. Ward . 2001. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4:10-13.
34. Hurst, J. L. 1990. Urine marking in populations of wild house mice Mus domesticus Rutty. I. Communication between males. Anim. Behav. 40:209-222.
35. Long, T. A. F., and R. Montgomerie . 2005. Ejaculate investment in a promiscuous rodent, Peromyscus maniculatus: effects of population density and social role. Evol. Ecol. Res. 8:345-356.
36. Lüpold, S., G. M. Linz, J. W. Rivers, D. F. Westneat, and T. R. Birkhead . 2009. Sperm competition selects beyond relative testes size in birds. Evolution 63:391-402.
37. Martin, P. A., T. J. Reimers, J. R. Lodge, and P. J. Dzuik . 1974. The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J. Reprod. Fertil. 39:251-258.
38. Mayhew, W. W., and S. J. Wright . 1970. Seasonal changes in testicular histology of three species of the lizard genus Uma. J. Morph. 130:163-185.
39. McLearn, K. R., and J. T. Manning . 1985. Mate choice, monogamy and mutational load. J. Theor. Biol. 116:369-376.
40. Montoto, L. G., M. Concepción, M. Tourmente, J. Martin-Coello, C. Crespo, J. J. Luque-Larena, M. Gomendio, and E. R. S. Roldan . 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS One 6:e18173.
41. Montoto, L. G., L. Arregui, N. M. Sanchez, M. Gomendio, and E. R. S. Roldan . 2012. Postnatal testicular development in mouse species with different levels of sperm competition. Reproduction 143:333-346.
42. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525-567.
43. Parker, G. A., and T. Pizzari . 2010. Sperm competition and ejaculate economics. Biol. Rev. 85:897-934.
44. Penn, D. J., and W. K. Potts . 1998. Chemical signals and parasite-mediated sexual selection. Trends Ecol. Evol. 13:391-396.
45. Peirce, E. J., and W. G. Breed . 2001. A comparative study of sperm production in two species of Australian arid zone rodents (Pseudomys australis, Notomys alexis) with marked differences in testis size. Reproduction 121:239-247.
46. Pitcher, T. E., P. O. Dunn, and L. A. Whittingham . 2005. Sperm competition and the evolution of testis size in birds. J. Evol. Biol. 18:557-567.
47. Pitnick, S., G. T. Miller, J. Reagan, and B. Holland . 2001. Males' evolutionary response to experimental removal of sexual selection. Proc. R. Soc. Lond. B Biol. Sci. 268:1071-1080.
48. Poiley, S. M. 1960. A systematic method of breeder rotation for non-inbred laboratory animal colonies. Proc. Anim. Care Panel 10:159-166.
49. Radwan, J. 2004. Effectiveness of sexual selection in removing mutations induced with ionization. Ecol. Let. 7:1149-1154.
50. Ramm, S. A., and L. Schärer . 2014. The evolutionary ecology of testicular function: size isn't everything. Biol. Rev. 89:874-888.
51. Ramm, S. A., and P. Stockley . 2009. Adaptive plasticity of mammalian sperm production in response to social experience. Proc. R. Soc. Lond. B Biol. Sci. 276:745-751.
52. Ramm, S. A. 2010. Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Lett. 6:219-221.
53. Ribble, D. O., and J. S. Millar . 1992. Intraspecific variation in testes size among northern populations of Peromyscus. Funct. Ecol. 6:455-459.
54. Roosen-Runge, E. C. 1977. The process of spermatogenesis in mammals. Cambridge Univ. Press, Cambridge, U.K.
55. Rowe, M., and S. Pruett-Jones . 2011. Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS One 6:e15720.
56. Russell, L. D., H. P. Ren, I. S. Hikim, W. Schulze, and A. P. S. Hikim . 1990. A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the Sertoli cell. Am. J. Anat. 188:21-30.
57. Schärer, L., P. Ladurner, and R. M. Rieger . 2004. Bigger testes do more work: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp. Behav. Ecol. Sociobiol. 56:420-425.
58. SciStat Calc. 2013. Levene's test: equality of variances. Available at: scistatcalc.blogspot.com. Accessed November 2, 2014.
59. Shabalina, S. A., L. Y. Yampolsky, and A. S. Kondrashov . 1997. Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc. Natl. Acad. Sci. USA 94:13034-13039.
60. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in insects. Princeton Univ. Press, Princeton, NJ.
61. Simmons, L. W., and F. Garcia-Gonzalez . 2008. Evolutionary reduction in testes size and competitive fertilisation success in response to the experimental removal of sexual selection in dung beetles. Evolution 62:2580-2591.
62. Stocco, D. M., and M. J. McPhaul . 2006. Physiology of testicular steroidogenesis. Pp. 977-1016 in J. D. Neill, T. M. Plant, D. W. Pfaff, J. R. G. Challis, D. M. De Krester, J. S. Richards, and P. M. Wassarman, eds. Knobil and Neill's physiology of reproduction. Vol. 1, 3rd ed. Academic Press, Burlington, MA.
63. Vrech D. E., P. A. Olivero, C. I. Mattoni, and A. V. Peretti . 2014. Testes mass, but not sperm length, increases with higher levels of polyandry in an ancient sex model. PLoS One 9:e94135.
64. Whitlock, M. C., and A. F. Agrawal . 2009. Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63:569-582.
65. Wistuba, J., A. Schrod, B. Grieve, J. K. Hodges, H. Aslam, G. F. Weinbauer, and C. M. Luetjens . 2003. Organization of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system. Biol. Reprod. 69:582-591.
66. Wistuba, J. A., J. Stukenborg, and M. Luetjens . 2007. Mammalian spermatogenesis. Funct. Develop. Embrol. 1:99-117.
67. Wolff, R. J. 1985. Mating behaviour and female choice: their relation to social status in wild caught house mice Mus musculus housed in a semi-natural environment. J. Zool. 207:43-51.