Phenotypic engineering of spermproductionrate confirms evolutionarypredictions of sperm competition theory

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1757, 2013, Pages

  Sekii, Kiyono ^a,b   Vizoso, Dita B ^a   Kuales, Georg ^c   De Mulder, Katrien ^a   Ladurner, Peter ^c,d   Schärer, Lukas ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Copulation frequency; Phenotypic engineering; RNA interference; Simultaneous hermaphrodite; Sperm competition; Sperm production

Indexed keywords

COPULATION; DOSE-RESPONSE RELATIONSHIP; EVOLUTIONARY THEORY; EXPERIMENTAL STUDY; FLATWORM; MALE BEHAVIOR; MATING BEHAVIOR; PATERNITY; PHENOTYPE; RNA; SPERM COMPETITION;

ANIMALIA; MACROSTOMUM LIGNANO; PLATYHELMINTHES;

EID: 84878437096     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2711     Document Type: Article

References (71)

1. Parker GA. 1970 Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-567. (doi:10.1111/j.1469-185X.1970. tb01176.x)
2. Birkhead TR, Pizzari T. 2002 Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262-273. (doi:10.1038/nrg774)
3. Parker GA. 1998 Sperm competition and the evolution of ejaculates: towards a theory base. In Sperm competition and sexual selection (eds TR Birkhead, AP Møller), pp. 3-54. London, UK: Academic Press.
4. Parker GA. 1990 Sperm competition games: raffles and roles. Proc. R. Soc. Lond. B 242, 120-126. (doi:10.1098/rspb.1990.0114)
5. Stockley P, Gage MJG, Parker GA, Møller AP. 1997 Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149, 933-954. (doi:10.1086/286031)
6. Pitcher TE, Dunn PO, Whittingham LA. 2005 Sperm competition and the evolution of testes size in birds. J. Evol. Biol. 18, 557-567. (doi:10.1111/j.1420-9101.2004.00874.x)
7. Møller AP, Briskie JV. 1995 Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36, 357-365. (doi:10.1007/BF00167797)
8. Møller AP. 1991 Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am. Nat. 137, 882-906. (doi:10.1086/ 285199)
9. Harcourt AH, Harvey PH, Larson SG, Short RV. 1981 Testis weight, body-weight and breeding system in primates. Nature 293, 55-57. (doi:10.1038/ 293055a0)
10. Ginsberg JR, Rubenstein DI. 1990 Sperm competition and variation in zebra mating-behavior. Behav. Ecol. Sociobiol. 26, 427-434. (doi:10.1007/BF00170901)
11. Parker GA, Pizzari T. 2010 Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934.
12. Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K. 2003 Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc. R. Soc. Lond. B 270, 633-640. (doi:10.1098/rspb.2002.2268)
13. Schulte-Hostedde AI, Millar JS. 2004 Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav. Ecol. Sociobiol. 55, 272-277. (doi:10.1007/s00265-003-0707-z)
14. Janicke T, Schärer L. 2009 Determinants of mating and sperm-transfer success in a simultaneous hermaphrodite. J. Evol. Biol. 22, 405-415. (doi:10.1111/j.1420-9101.2008.01660.x)
15. Bercovitch FB, Nurnberg P. 1996 Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). J. Reprod. Fertil. 107, 59-68. (doi:10.1530/jrf.0.1070059)
16. Awata S, Heg D, Munehara H, Kohda M. 2006 Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus. Behav. Ecol. 17, 372-379. (doi:10.1093/beheco/arj043)
17. Hosken DJ, Garner TWJ, Ward PI. 2001 Sexual conflict selects for male and female reproductive characters. Curr. Biol. 11, 489-493. (doi:10.1016/ S0960-9822(01)00146-4)
18. Hosken DJ, Ward PI. 2001 Experimental evidence for testes size evolution via sperm competition. Ecol. Lett. 4, 10-13. (doi:10.1046/j.1461-0248.2001.00198.x)
19. Pitnick S, Miller GT, Reagan J, Holland B. 2001 Males' evolutionary responses to experimental removal of sexual selection. Proc. R. Soc. Lond. B 268, 1071-1080. (doi:10.1098/rspb.2001.1621)
20. Simmons LW, Garcia-Gonzalez F. 2008 Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evol. Int. J. Organ. Evol. 62, 2580-2591. (doi:10.1111/j.1558-5646.2008.00479.x)
21. Dewsbury DA. 1982 Ejaculate cost and male choice. Am. Nat. 119, 601-610. (doi:10.1086/283938)
22. Nakatsuru K, Kramer DL. 1982 Is sperm cheap? Limited male-fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216, 753-755. (doi:10.1126/science.216.4547.753)
23. Van Voorhies WA. 1992 Production of sperm reduces nematode life-span. Nature 360, 456-458. (doi:10.1038/360456a0)
24. Olsson M, Madsen T, Shine R. 1997 Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264, 455-459. (doi:10.1098/rspb.1997.0065)
25. Wedell N, Gage MJG, Parker GA. 2002 Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313-320. (doi:10.1016/S0169-5347(02)02533-8)
26. Reinhardt K, Naylor R, Siva-Jothy MT. 2011 Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius. PLoS ONE 6, e22082. (doi:10.1371/journal.pone.0022082)
27. Lemaitre JF, Rigaud T, Cornet S, Bollache L. 2009 Sperm depletion, male mating behaviour and reproductive 'time-out' in Gammarus pulex (Crustacea, Amphipoda). Anim. Behav. 77, 49-54. (doi:10.1016/j.anbehav.2008.08.028)
28. Van Son TC, Thiel M. 2006 Mating behaviour of male rock shrimp, Rhynchocinetes typus (Decapoda: Caridea): effect of recent mating history and predation risk. Anim. Behav. 71, 61-70. (doi:10.1016/j.anbehav.2005.03.018)
29. Hettyey A, Vági B, Hévizi G, Török J. 2009 Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biol. J. Linnean Soc. 96, 361-371. (doi:10.1111/j. 1095-8312.2008.01126.x)
30. Hodgkin J, Barnes TM. 1991 More is not better: brood size and population-growth in a selffertilizing nematode. Proc. R. Soc. Lond. B 246, 19-24. (doi:10.1098/rspb.1991.0119)
31. Andersson M. 1982 Female choice selects for extreme tail length in a widowbird. Nature 299, 818-820. (doi:10.1038/299818a0)
32. Møller AP. 1988 Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 332, 640-642. (doi:10.1038/332640a0)
33. Polak M, Rashed A. 2010 Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc. R. Soc. B 277, 1371-1376. (doi:10.1098/rspb.2009.1720)
34. Maklakov AA, Arnqvist G. 2009 Testing for direct and indirect effects of mate choice by manipulating female choosiness. Curr. Biol. 19, 1903-1906. (doi:10.1016/j.cub.2009.08.058)
35. Kuales G, De Mulder K, Glashauser J, Salvenmoser W, Takashima S, Hartenstein V, Berezikov E, Salzburger W, Ladurner P. 2011 Boule-like genes regulate male and female gametogenesis in the flatworm Macrostomum lignano. Dev. Biol. 357, 117-132. (doi:10.1016/j.ydbio.2011.06.030)
36. Ladurner P, Egger B, De Mulder K, Pfister D, Kuales G, Salvenmoser W, Schärer L. 2008 The stem cell system of the basal flatworm Macrostomum lignano. In Stem cells: from hydra to man (ed. TCG Bosch), pp. 75-94. Berlin, Germany: Springer.
37. Schärer L, Ladurner P. 2003 Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proc. R. Soc. Lond. B 270, 935-941. (doi:10.1098/rspb.2002.2323)
38. Schärer L, Janicke T. 2009 Sex allocation and sexual conflict in simultaneously hermaphroditic animals. Biol. Lett. 5, 705-708. (doi:10.1098/rsbl.2009.0100)
39. Schärer L, Vizoso DB. 2007 Phenotypic plasticity in sperm production rate: there's more to it than testis size. Evol. Ecol. 21, 295-306. (doi:10.1007/s10682- 006-9101-4)
40. Sekii K, Salvenmoser W, De Mulder K, Schärer L, Ladurner P. 2009 Melav2, an elav-like gene, is essential for spermatid differentiation in the flatworm Macrostomum lignano. BMC Dev. Biol. 9, 62. (doi:10.1186/1471-213X-9-62)
41. Pfister D, De Mulder K, Hartenstein V, Kuales G, Borgonie G, Marx F, Morris J, Ladurner P. 2008 Flatworm stem cells and the germ line: developmental and evolutionary implications of macvasa expression in Macrostomum lignano. Dev. Biol. 319, 146-159. (doi:10.1016/j.ydbio. 2008.02.045)
42. Janicke T, Kesselring H, Schärer L. 2012 Strategic mating effort in a simultaneous hermaphrodite: the role of the partner's feeding status. Behav. Ecol. Sociobiol. 66, 593-601. (doi:10.1007/s00265-011- 1307-y)
43. Ladurner P, Schärer L, Salvenmoser W, Rieger RM. 2005 A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha). J. Zool. Syst. Evol. Res. 43, 114-126. (doi:10.1111/j.1439-0469.2005.00299.x)
44. Schärer L, Joss G, Sandner P. 2004 Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar. Biol. 145, 373-380. (doi:10.1007/s00227-004-1314-x)
45. Andersen RA, Berges JA, Harrison PJ, Watanabe MM. 2005 Recipes for freshwater and seawater media. In Algal culturing techniques (ed. RA Andersen), pp. 429-538. Amsterdam, The Netherlands: Elsevier.
46. Rieger RM, Gehlen M, Haszprunar G, Holmlund M, Legniti A, Salvenmoser W, Tyler S. 1988 Laboratory cultures of marine Macrostomida (Turbellaria). Fortschr. Zool. 36, 523.
47. Yen PH. 2004 Putative biological functions of the DAZ family. Int. J. Androl. 27, 125-129. (doi:10.1111/j.1365-2605.2004.00469.x)
48. Shah C, VanGompel MJW, Naeem V, Chen YM, Lee T, Angeloni N, Wang Y, Xu EY. 2010 Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function. Plos Genet. 6, e1001022. (doi:10.1371/journal.pgen.1001022)
49. Krackow S, Tkadlec E. 2001 Analysis of brood sex ratios: implications of offspring clustering. Behav. Ecol. Sociobiol. 50, 293-301(doi:10.1007/ s002650100366)
50. Wilson K, Hardy ICW. 2002 Statistical analysis of sex ratios: an introduction. In Sex ratios (ed. ICW Hardy), pp. 48-92. Cambridge, UK: Cambridge University Press.
51. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. 2009 Mixed effects models and extensions in ecology with r (statistics for biology and health). Berlin, Germany: Springer.
52. Crawley MJ. 2005 Statistics: an introduction using R. New York, NY: Wiley.
53. Johnson RK, Eckardt GR, Rathje TA, Drudik DK. 1994 10 generations of selection for predicted weight of testes in swine-direct response and correlated response in body-weight, backfat, age at puberty, and ovulation rate. J. Anim. Sci. 72, 1978-1988.
54. Rathje TA, Johnson RK, Lunstra DD. 1995 Sperm production in boars after 9 generations of selection for increased weight of testis. J. Anim. Sci. 73, 2177-2185.
55. Tan GN, Govedich FR, Burd M. 2004 Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae). J. Evol. Biol. 17, 574-580. (doi:10.1111/j.1420-9101.2004.00692.x)
56. Schärer L. 2009 Tests of sex allocation theory in simultaneously hermaphroditic animals. Evol. Int. J. Organ. Evol. 63, 1377-1405. (doi:10.1111/j. 1558-5646.2009.00669.x)
57. Tatar M. 2000 Transgenic organisms in evolutionary ecology. Trends Ecol. Evol. 15, 207-211. (doi:10.1016/S0169-5347(00)01834-6)
58. Charnov EL. 1982 The theory of sex allocation. Princeton, NJ: Princeton University Press.
59. Petersen CW. 1991 Sex allocation in hermaphroditic seabasses. Am. Nat. 138, 650-667. (doi:10.1086/285240)
60. Schärer L, Pen I. 2013 Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition. Phil. Trans. R. Soc. B 368, 20120052. (doi:10.1098/rstb.2012.0052)
61. Marie-Orleach L, Janicke T, Schärer L. 2013 Effects of mating status on post-copulatory behaviour in a simultaneous hermaphrodite. Animal Behaviour 85, 453-461.
62. Dewsbury DA. 1981 Effects of novelty on copulatory behavior-the Coolidge effect and related phenomena. Psychol. Bull. 89, 464-482. (doi:10.1037/0033-2909.89.3.464)
63. Wilson JR, Kuehn RE, Beach FA. 1963 Modification in the sexual behavior of male rats produced by changing the stimulus female. J. Comp. Physiol. Psychol. 56, 636-644. (doi:10.1037/h0042469)
64. Brown RE. 1974 Sexual arousal, the Coolidge effect and dominance in the rat (Rattus norvegicus). Anim. Behav. 22, 634-637. (doi:10.1016/S0003-3472(74)80009-6)
65. Steiger S, Franz R, Eggert AK, Müller JK. 2008 The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle. Proc. R. Soc. B 275, 1831-1838. (doi:10.1098/rspb.2008.0375)
66. Koene JM, Ter Maat A. 2007 Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite. BMC Evol. Biol. 7, 212. (doi:10.1186/1471-2148-7-212)
67. Moreira JR, Macdonald DW, Clarke JR. 1997 Correlates of testis mass in capybaras (Hydrochaeris hydrochaeris): dominance assurance or sperm competition? J. Zool. 241, 457-463. (doi:10.1111/j.1469-7998.1997.tb04837.x)
68. Murray RL, Cutter AD. 2011 Experimental evolution of sperm count in protandrous self-fertilizing hermaphrodites. J. Exp. Biol. 214, 1740-1747. (doi:10.1242/jeb.053181)
69. Boschetto C, Gasparini C, Pilastro A. 2011 Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65, 813-821. (doi:10.1007/s00265- 010-1085-y)
70. Vizoso DB, Rieger G, Schärer L. 2010 Goings-on inside a worm: functional hypotheses derived from sexual conflict thinking. Biol. J. Linnean Soc. 99, 370-383. (doi:10.1111/j.1095-8312.2009.01363.x)
71. Demircan T, De Mulder K, Simanov D, Glashauser J, Vizoso VB, Schärer L, Ladurner P, Berezikov E. In preparation. Stable transgenic lines of the regenerating flatworm Macrostomum lignano.