Convergence, recurrence and diversification of complex sperm traits in diving beetles (Dytiscidae)

Evolution

Volumn 66, Issue 5, 2012, Pages 1650-1661

  Higginson, Dawn M ^a,c   Miller, Kelly B ^b   Segraves, Kari A ^a   Pitnick, Scott ^a  

^a SYRACUSE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Ornament evolution; Postcopulatory reproductive traits; Sexual selection; Sperm conjugation; Sperm heteromorphism

Indexed keywords

BEETLE; CONVERGENCE; DIVERGENCE; MORPHOLOGY; PHYLOGENETICS; SEXUAL SELECTION; SPERM;

ANIMAL; ARTICLE; BAYES THEOREM; BEETLE; BIOLOGICAL MODEL; CYTOLOGY; EVOLUTION; GENETICS; HISTOLOGY; MALE; MONTE CARLO METHOD; PHYLOGENY; PHYSIOLOGY; PROBABILITY; SPERMATOZOON;

ANIMALS; BAYES THEOREM; BEETLES; BIOLOGICAL EVOLUTION; MALE; MARKOV CHAINS; MODELS, GENETIC; MONTE CARLO METHOD; PHYLOGENY; SPERMATOZOA;

COLEOPTERA; DYTISCIDAE; HYGROBIIDAE;

EID: 84859120649     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01532.x     Document Type: Article

References (75)

1. Aiken, R. B. 1992. The mating behaviour of a boreal water beetle, Dytiscus alaskanus (Coleopotera Dytiscidae). Ethol. Ecol. Evol. 4:245-254.
2. Aiken, R. B., and W. Wilkinson 1985. Bionomics of Dytiscus alaskanus J. Balfour-Browne (Coleoptera: Dytiscidae) in a central Alberta lake. Can. J. Zool. 63:1316-1323.
3. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ
4. Auerbach, L. 1893. Remarkable behaviour of the spermatozoa of Dytiscus marginalis. J. R. Microsc. Soc. 13:622.
5. Ballowitz, E. 1895. Die dopplespermatozoen der Dyticiden. Zeitschrift für Wissenschaftliche Zoologie 60:458-499.
6. Bergsten, J., and K. B. Miller 2007. Phylogeny of diving beetles reveals a coevolutionary arms race between the sexes. PloS One 2:e522.
7. Birkhead, T. R. 2000. Defining and demonstrating postcopulatory female choice-again. Evolution 54:1057-1060.
8. Boughman, J. W., H. D. Rundle, and D. Schluter 2005. Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361-373.
9. Breed, W. G. 2005. Evolution of the spermatozoon in muroid rodents. J. Morphol. 265:271-290.
10. Cleavall, L. M. 2009. Description of Thermonectus nigrofasciatus and Rhantus binotatus (Coleoptera: Dytiscidae) mating behavior. Pp. 34. MS Thesis. University of New Mexico, Albuquerque
11. Emlen, D. J., J. Marangelo, B. Ball, and C. W. Cunningham 2005. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060-1084.
12. Fitzpatrick, J. L., R. Montgomerie, J. K. Desjardins, K. A. Stiver, N. Kolm, and S. Balshine 2009. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl. Acad. Sci. USA 106:1128-1132.
13. Gage, M. J. G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc. R. Soc. Lond. B 258:247-254.
14. Gomendio, M., and E. R. S. Roldan 1991. Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B 243:181-185.
15. Harcourt, A. H., P. H. Harvey, D. J. Larson, and R. V. Short 1981. Testis weight, body weight and breeding system in primates. Nature 293:55-57.
16. Hayashi, F. 1998. Sperm co-operation in the fishfly, Parachauliodes japonicus. Funct. Ecol. 12:347-350.
17. Henry, C. S., M. L. M. Wells, and C. M. Simon 1999. Convergent evolution of courtship songs among cryptic species of the Carnea group of green lacewings (Neuroptera: Chrysopidae: Chrysoperla). Evolution 53:1165-1179.
18. Higginson, D. M., and S. Pitnick 2011. Evolution of intra-ejaculate sperm interactions: do sperm cooperate? Biol. Rev. 87:249-270.
19. Immler, S. 2008. Sperm competition and sperm cooperation: the potential role of diploid and haploid expression. Reproduction 135:275-283.
20. Immler, S., H. D. M. Moore, W. G. Breed, and T. R. Birkhead 2007. By hook or by crook? Morphometry, competition and cooperation in rodent sperm. PloS One 2:e170.
21. Inoda, T. 2003. Mating and reproduction of predaceous diving beetles, Dytiscus sharpi, observed under artificial breeding conditions. Zool. Sci. 20:377-382.
22. Inoda, T., F. Tajima, H. Taniguchi, M. Saeki, K. Numakura, M. Hasegawa, and S. Kamimura 2007. Temperature-dependent regulation of reproduction in the diving beetle Dytiscus sharpi (Coleoptera: Dytiscidae). Zool. Sci. 24:1115-1121.
23. Jamieson, B. G. M., R. Dallai, and B. A. Afzelius 1999. Insects: their spermatozoa and phylogeny. Science Publishers, Inc., Enfield
24. Keller, L., and H. K. Reeve 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv. Stud. Behav. 24:291-315.
25. Kraaijeveld, K., F. J. L. Kraaijeveld-Smit, and M. E. Maan 2011. Sexual selection and speciation: the comparative evidence revisited. Biol. Rev. 86:367-377.
26. Landan, G., and D. Graur 2007. Heads or tails: a simple reliability check for multiple sequence alignments. Mol. Biol. Evol. 24:1380-1383.
27. Lighthill, J. 1976. Flagellar hydrodynamics. SIAM Rev. 18:161-230.
28. Löytynoja, A., and N. Goldman 2008. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science 320:1632-1635.
29. Meyer, A., J. M. Morrissey, and M. Schartl 1994. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368:539-542.
30. Miller, K. B. 2001. On the phylogeny of the Dytiscidae (Insecta: Coleoptera) with emphasis on the morphology of the female reproductive system. Insect Syst. Evol. 31:45-92.
31. Miller, K. B.. 2003. The phylogeny of diving beetles (Coleoptera: Dytiscidae) and the evolution of sexual conflict. Biol. J. Linn. Soc. 79:359-388.
32. Miller, G. T., and S. Pitnick 2002. Sperm-female coevolution in Drosophila. Science 298:1230-1233.
33. Minin, V., Z. Abdo, P. Joyce, and J. Sullivan 2003. Performance-based selection of likelihood models for phylogeny estimation. Syst. Biol. 52:674-683.
34. Møller, A. P., and J. V. Briskie 1995. Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36:357-365.
35. Moore, H., K. Dvořáková, N. Jenkins, and W. Breed 2002. Exceptional sperm cooperation in the wood mouse. Nature 418:174-177.
36. Moore, H. D. M., and D. A. Taggart 1995. Sperm pairing in the opossum increases the efficiency of sperm movement in a viscous environment. Biol. Reprod. 52:947-953.
37. Nilsson, A. N. 2000. A new view on the generic classification of the Agabus-group of genera of the Agabini, aimed at solving the problem with a paraphyletic Agabus (Coleoptera: Dytiscidae). Koleopterol. Rundsch. 70:17-36.
38. Nilsson, A. N. 2001. Dytiscidae. World Catalogue of Insects. Vol. 3. Apollo Books Aps., Stenstrup
39. Nilsson, A. N., and H. Fery 2006. World catalogue of Dytiscidae-corrections and additions, 3. Koleopterol. Rundsch. 76:55-74.
40. Nylander, J. A. A., J. C. Wilgenbusch, D. L. Warren, and D. L. Swofford 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581-583.
41. Omland, K. E., and S. M. Lanyon 2000. Reconstructing plumage evolution in Orioles (Icterus): repeated convergence and reversal in patterns. Evolution 54:2119-2133.
42. Pagel, M. 2000. Discrete, version 4.0
43. Pagel, M.. 2002. Multistate
44. Pagel, M., and A. Meade 2006a. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167:808-825.
45. Pagel, M., and A. Meade 2006b. BayesTraits
46. Pagel, M., A. Meade, and D. Barker 2004. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53:673-684.
47. Pattarini, J. M., W. T. Starmer, A. Bjork, and S. Pitnick 2006. Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60:2064-2080.
48. Pitnick, S. 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148:57-90.
49. Pitnick, S., and W. D. Brown 2000. Criteria for demonstrating female sperm choice. Evolution 54:1052-1056.
50. Pitnick, S., T. A. Markow, and G. S. Spicer 1995. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl. Acad. Sci. USA 92:10614-10618.
51. Pitnick, S., D. J. Hosken, and T. R. Birkhead 2009a. Sperm morphological diversity. Pp. 69-149 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology, an evolutionary perspective. Academic Press, San Diego, CA
52. Pitnick, S., M. F. Wolfner, and S. S. Suarez 2009b. Ejaculate-female and sperm-female interactions. Pp. 247-304 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology, an evolutionary perspective. Academic Press, San Diego, CA
53. Pizzari, T., and T. R. Birkhead 2002. The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol. Rev. 77:183-209.
54. Pizzari, T., and K. R. Foster 2008. Sperm sociality: cooperation, altruism, and spite. PLoS Biol. 6:e130.
55. Pizzari, T., and G. A. Parker 2009. Sperm competition and sperm phenotype. Pp. 205-244 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology, an evolutionary perspective. Elsevier, London
56. Prager, M., and S. Andersson 2010. Convergent evolution of red carotenoid coloration in widowbirds and bishops (Euplectes spp.). Evolution 64:3609-3619.
57. Price, J. J., N. R. Friedman, and K. E. Omland 2007. Song and plumage evolution in the new world orioles (Icterus) show similar lability and convergence in patterns. Evolution 61:850-863.
58. Prum, R. O. 1997. Phylogenetic tests of alternative intersexual selection mechanisms: trait macroevolution in a polygynous clade (Aves: Pipridae). Am. Nat. 149:668-692.
59. Prum, R. O. 2010. The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: implications for the meaning, honesty, and design in intersexual signals. Evolution 64:3085-3100.
60. Puniamoorthy, N., M. R. B. Ismail, D. S. H. Tan, and R. Meier 2009. From kissing to belly stridulation: comparative analysis reveals surprising diversity, rapid evolution, and much homoplasy in the mating behaviour of 27 species of sepsid flies (Diptera: Sepsidae) J. Evol. Biol. 22:2146-2156.
61. Rasband, W. S. 19972008. ImageJ. U.S. National Institutes of Health, Bethesda, MD
62. Ribera, I., A. P. Vogler, and M. Balke 2008. Phylogeny and diversification of diving beetles (Coleoptera: Dytiscidae). Cladistics 23:1-28.
63. Roldan, E. R. S., M. Gomendio, and A. D. Vitullo 1992. The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biol. Rev. 67:551-593.
64. Ronquist, F., and J. P. Huelsenbeck 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
65. Schärer, L., G. Joss, and P. Sandner 2004. Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar. Biol. 145:373-380.
66. Schärer, L., D. T. J. Littlewood, A. Waeschenbach, W. Yoshida, and D. B. Vizoso 2011. Mating behavior and the evolution of sperm design. Proc. Natl. Acad. Sci. USA 108:1490-1495.
67. Schulter, D., T. Price, A. Ø. Mooers, and D. Ludwig 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699-1711.
68. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton Univ. Press, Princeton, NJ
69. Smith, R. L. 1973. Aspects of the biology of three species of the genus Rhantus (Coleoptera: Dytiscidae) with special reference to the acoustical behavior of two. Can. Entomol. 105:909-919.
70. Snook, R. R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20:46-53.
71. Stockley, P., M. J. G. Gage, G. A. Parker, and A. P. Møller 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149:933-954.
72. * and other methods). Version 4. Sinauer Associates, Sunderland, MA
73. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford Univ. Press, New York
74. Wiens, J. J. 2001. Widespread loss of sexually selected traits: how the peacock lost its spots. Trends Ecol. Evol. 16:517-523.
75. Woolley, D. M., R. F. Crockett, W. D. I. Groom, and S. G. Revell 2009. A study of synchronisation between the flagella of bull spermatozoa, with related observations. J. Exp. Biol. 212:2215-2223.