Someone like me: Size-assortative pairing and mating in an Amazonian fish, sailfin tetra Crenuchus spilurus

English version

Autoři: Elio de Almeida Borghezan ^aff001; Kalebe da Silva Pinto ^aff001; Jansen Zuanon ^aff001; Tiago Henrique da Silva Pires ^aff001
Působiště autorů: Laboratório de Ecologia Comportamental e Evolução, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, Manaus, AM, Brazil ^aff001; Wildlife Research Center of Kyoto University, Sakyo-ku, Kyoto, Japan ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222880

Souhrn

In the absence of constraints, preference for larger mates is expected to evolve, as larger individuals are typical of higher potential fitness. Large females are often more fecund and carry larger eggs (which result in higher number and better quality of offspring), whereas large males usually have more conspicuous ornaments and are better at defending resources. However, intrasexual competition can constrain the access to larger partners, especially when opportunities for mate takeover abound. Here we investigate the relationship between individual’s size and mate choice in relation to one’s own size and their respective mate’s size using the sailfin tetra, a sexually dimorphic Amazonian fish species. We show that ornaments of larger males are exponentially more conspicuous, and larger females are more fecund and carry larger eggs. Contrary to expectation, neither males nor females associated for longer with the larger of two offered potential mates. Instead, individuals of both genders chose opposite-sex individuals of similar sizes to themselves. Additionally, similar-sized pairs were more likely to spawn than couples with higher size asymmetries. Grounded on field observations, we propose that prudent choice should be particularly important in this system, since courtship is long (often taking several days), which offers opportunities for mate takeover. Intrasexual competition, however, cannot readily explain female choice for similar-sized males. We thus suggest that such preference might be best explained by avoidance of filial cannibalism.

Klíčová slova:

Fecundity – Fish – Natural selection – Oocytes – Physiological parameters – Predation – Spawning – Swimming

Zdroje

1. Baldauf SA, Kullmann H, Schroth SH, Thünken T, Bakker TCM. You can’t always get what you want: Size assortative mating by mutual mate choice as a resolution of sexual conflict. BMC Evol Biol. 2009;9: 129. doi: 10.1186/1471-2148-9-129 19515244

2. Crespi BJ. Causes of assortative mating in arthropods. Anim Behav. 1989; doi: 10.1016/S0003-3472(89)80138-1

3. Jiang Y, Bolnick DI, Kirkpatrick M. Assortative mating in animals. Am Nat. 2013;181: E125–E138. doi: 10.1086/670160 23669548

4. Pryke SR, Griffith SC. The relative role of male vs. female mate choice in maintaining assortative pairing among discrete colour morphs. J Evol Biol. 2007;20: 1512–1521. doi: 10.1111/j.1420-9101.2007.01332.x 17584244

5. Shine R, O’connor D, Lemaster MP, Mason RT. Pick on someone your own size: ontogenetic shifts in mate choice by male garter snakes result in size-assortative mating. Anim Behav. 2001;61: 1133–1141. doi: 10.1006/anbe.2001.1712

6. Bortolotti GR, González LM, Margalida A, Sánchez R, Oria J. Positive assortative pairing by plumage colour in Spanish imperial eagles. Behav Processes. 2008;78: 100–107. doi: 10.1016/j.beproc.2008.01.007 18295983

7. Ferrer M, Penteriani V. A process of pair formation leading to assortative mating: passive age-assortative mating by habitat heterogeneity. Anim Behav. 2003;66: 137–143. doi: 10.1006/anbe.2003.2158

8. Ludwig SC, Becker PH. Supply and demand: Causes and consequences of assortative mating in common terns Sterna hirundo. Behav Ecol Sociobiol. 2008;62: 1601–1611. doi: 10.1007/s00265-008-0589-1

9. Holveck M-J, Riebel K. Low-quality females prefer low-quality males when choosing a mate. Proc R Soc B Biol Sci. 2010;277: 153–160. doi: 10.1098/rspb.2009.1222 19812084

10. Michiels NK, Hohner A, Vorndran IC. Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons? Behav Ecol. 2001;12: 612–618. doi: 10.1093/beheco/12.5.612

11. Harari A, Handler A, Landolt P. Size-assortative mating, male choice and female choice in the curculionid beetle Diaprepes abbreviatus. Anim Behav. 1999;58: 1191–1200. doi: 10.1006/anbe.1999.1257 10600139

12. Bel-Venner M., Dray S, Allaine D, Menu F, Venner S. Unexpected male choosiness for mates in a spider. Proc R Soc B Biol Sci. 2008;275: 77–82. doi: 10.1098/rspb.2007.1278 17956845

13. Wada S, Arashiro Y, Takeshita F, Shibata Y. Male mate choice in hermit crabs: Prudence by inferior males and simple preference by superior males. Behav Ecol. 2010;22: 114–119. doi: 10.1093/beheco/arq183

14. Helfenstein F, Danchin E, Wagner RH. Assortative mating and sexual size dimorphism in black-legged kittiwakes. Waterbirds Int J Waterbird Biol. 2004;27: 350–354. doi: 10.1675/1524-4695(2004)027[0350:AMASSD]2.0.CO;2

15. Pack AA, Herman LM, Spitz SS, Craig AS, Hakala S, Deakos MH, et al. Size-assortative pairing and discrimination of potential mates by humpback whales in the Hawaiian breeding grounds. Anim Behav. 2012;84: 983–993. doi: 10.1016/j.anbehav.2012.07.024

16. Galipaud M, Bollache L, Dechaume-Moncharmont FX. Assortative mating by size without a size-based preference: The female-sooner norm as a mate-guarding criterion. Anim Behav. 2013;85: 35–41. doi: 10.1016/j.anbehav.2012.09.038

17. Taborsky B, Guyer L, Taborsky M. Size-assortative mating in the absence of mate choice. Anim Behav. 2009;77: 439–448. doi: 10.1016/j.anbehav.2008.10.020

18. Brown WD. Size-assortative mating in the blister beetle Lytta magister (Coleoptera: Meloidae) is due to male and female preference for larger mates. Anim Behav. 1990;40: 901–909. doi: 10.1016/S0003-3472(05)80992-3

19. Johnstone RA, Reynolds JD, Deutsch JC. Mutual mate choice and sex differences in choosiness. Evolution (NY). 1996;50: 1382–1391. doi: 10.2307/2410876

20. Trivers RLL. Parental investment and sexual selection. Sexual selection and the descent of man. 1972. pp. 136–179. doi: 10.1002/ajpa.1330400226

21. Briffa M, Elwood RW. Repeated measures analysis of contests and other dyadic interactions: problems of semantics, not statistical validity. Anim Behav. 2010;80: 583–588. doi: 10.1016/j.anbehav.2010.06.009

22. Sacchi R, Pupin F, Gentilli A, Rubolini D, Scali S, Fasola M, et al. Male-male combats in a polymorphic lizard: Residency and size, but not color, affect fighting rules and contest outcome. Aggress Behav. 2009;35: 274–283. doi: 10.1002/ab.20305 19291744

23. Rowland WJ. The effects of body size, aggression and nuptial coloration on competition for territories in male threespine sticklebacks, Gasterosteus aculeatus. Anim Behav. 1989;37: 282–289. doi: 10.1016/0003-3472(89)90117-6

24. Taborsky B, Guyer L, Demus P. “Prudent habitat choice”: A novel mechanism of size-assortative mating. J Evol Biol. 2014;27: 1217–1228. doi: 10.1111/jeb.12398 24801110

25. Bisazza A, Marconato A. Female mate choice, male-male competition and parental care in the river bullhead, Cottus gobio L. (Pisces, Cottidae). Anim Behav. 1988;36: 1352–1360. doi: 10.1016/S0003-3472(88)80204-5

26. Gagliardi-Seeley JL, Itzkowitz M. Male size predicts the ability to defend offspring in the biparental convict cichlid Archocentrus nigrofasciatus. J Fish Biol. 2006;69: 1239–1244. doi: 10.1111/j.1095-8649.2006.01174.x

27. Oliveira RF, Miranda J a, Carvalho N, Gonçalves EJ, Grober MS, Santos RS. Male mating success in the Azorean rock-pool blenny: The effects of body size, male behaviour and nest characteristics. J Fish Biol. 2000;57: 1416–1428. doi: 10.1006/jfbi.2000.1403

28. Côte IM, Hunte W. Male and female mate choice in the redlip blenny: Why bigger is better. Anim Behav. 1989;38: 78–88. doi: 10.1016/S0003-3472(89)80067-3

29. Darwin C. The descent of man and selection in relation to sex. London; 1871.

30. Prum RO. Aesthetic evolution by mate choice: Darwin’s really dangerous idea. Philos Trans R Soc B Biol Sci. 2012;367: 2253–2265. doi: 10.1098/rstb.2011.0285 22777014

31. Rosenthal GG, Evans CS. Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc Natl Acad Sci U S A. 1998;95: 4431–4436. doi: 10.1073/pnas.95.8.4431 9539754

32. Andersson M. Sexual Selection. New Jersey: Princeton University Press;1994.

33. Kodric-Brown A, Sibly RM, Brown JH. The allometry of ornaments and weapons. Proc Natl Acad Sci U S A. 2006;103: 8733–8738. doi: 10.1073/pnas.0602994103 16731616

34. Barry KL, Kokko H. Male mate choice: Why sequential choice can make its evolution difficult. Anim Behav. 2010;80: 163–169. doi: 10.1016/j.anbehav.2010.04.020

35. Kokko H, Johnstone RA. Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc B Biol Sci. 2002;357: 319–330. doi: 10.1098/rstb.2001.0926 11958700

36. Edward DA, Chapman T. The evolution and significance of male mate choice. Trends Ecol Evol. 2011;26: 647–654. doi: 10.1016/j.tree.2011.07.012 21890230

37. Parker GA, Simmons LW. Parental investment and the control of sexual selection, predictiong the direction of sexual competition. Proc Biol Sci. 1996;263: 315–321. doi: 10.1098/rspb.1996.0078

38. Clutton-Brock TH. Reproductive success: Studies of individual variation in contrasting breeding systems. Chicago: University of Chicago Press; 1988.

39. Honek A. Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos. 1993;66: 483–492. doi: 10.2307/3544943

40. Dosen LD, Montgomerie R. Female size influences mate preferences of male guppies. Ethology. 2004;110: 245–255. doi: 10.1111/j.1439-0310.2004.00965.x

41. Herdman EJE, Kelly CD, Godin JGJ. Male mate choice in the guppy (Poecilia reticulata): Do males prefer larger females as mates? Ethology. 2004;110: 97–111. doi: 10.1111/j.1439-0310.2003.00960.x

42. Olsson M. Male preference for large females and assortative mating for body size in the sand lizard (Lacerta agilis). Behav Ecol Sociobiol. 1993;32: 337–341. doi: 10.1007/BF00183789

43. Werner NY, Lotem A. Choosy males in a haplochromine cichlid: First experimental evidence for male mate choice in a lekking species. Anim Behav. 2003;66: 293–298. doi: 10.1006/anbe.2003.2208

44. Henry LM. Assortative mating and the role of phenotypic plasticity in male competition: implications for gene flow among host-associated parasitoid populations. Biol Lett. 2008;4: 508–511. doi: 10.1098/rsbl.2008.0369 18700194

45. Whiteman EA, Côté IM. Social monogamy in the cleaning goby Elacatinus evelynae: Ecological constraints or net benefit? Anim Behav. 2003;66: 281–291. doi: 10.1006/anbe.2003.2200

46. Candolin U, Salesto T. Does competition allow male mate choosiness in threespine sticklebacks? Am Nat. 2009;173: 273–277. doi: 10.1086/595753 19117472

47. Hume KD, Elwood RW, Dick JTA, Connaghan KM. Size-assortative pairing in Gammarus pulex (Crustacea: Amphipoda): A test of the timing hypothesis. Anim Behav. 2002;64: 239–244. doi: 10.1006/anbe.2002.3045

48. Venner S, Bernstein C, Dray S, Bel‐Venner M. Make love not war: When should less competitive males choose low‐quality but defendable females? Am Nat. 2010;175: 650–661. doi: 10.1086/652432 20415532

49. Bel-Venner MC, Venner S. Mate-guarding strategies and male competitive ability in an orb-weaving spider: Results from a field study. Anim Behav. 2006;71: 1315–1322. doi: 10.1016/j.anbehav.2005.08.010

50. Elwood R, Gibson J, Neil S. The amorous Gammarus: Size assortative mating in G. pulex. Anim Behav. 1987;35: 1–6. doi: 10.1016/S0003-3472(87)80203-8

51. Fawcett TW, Johnstone RA. Mate choice in the face of costly competition. Behav Ecol. 2003;14: 771–779. doi: 10.1093/beheco/arg075

52. Franceschi N, Lemaître JF, Cézilly F, Bollache L. Size-assortative pairing in Gammarus pulex (Crustacea: Amphipoda): A test of the prudent choice hypothesis. Anim Behav. 2010;79: 911–916. doi: 10.1016/j.anbehav.2010.01.002

53. Härdling R, Kokko H. The evolution of prudent choice. Evol Ecol Res. 2005;7: 697–715. doi: 10.1046/j.1461-0248.1999.00075.x

54. Le Boeuf BJ. Male-male competition and reproductive success in elephant seals. Am Zool. 1974;14: 163–176.

55. Masonjones HD, Lewis SM. Courtship behavior in the dwarf seahorse, Hippocampus zosterae. Copeia. 1996;1996: 634–640. doi: 10.2307/1447527

56. Pires THS, Farago TB, Campos DF, Cardoso GM, Zuanon J. Traits of a lineage with extraordinary geographical range: Ecology, behavior and life-history of the sailfin tetra Crenuchus spilurus. Environ Biol Fishes. 2016;99: 925–937. doi: 10.1007/s10641-016-0534-5

57. Ridley M, Thompson DJ. Size and mating in Asellus aquaticus (Crustacea: Isopoda). Ethology. 1979;51: 380–397.

58. Pires THS, Borghezan EA, Machado VN, Powell DL, Röpke CP, Oliveira C, et al. Testing Wallace’s intuition: Water type, reproductive isolation and divergence in an Amazonian fish. J Evol Biol. 2018;31: 882–892. doi: 10.1111/jeb.13272 29577482

59. Pires THS, Borghezan EA, Cunha SLR, Leitão RP, Pinto KS, Zuanon J. Sensory drive in colourful waters: Morphological variation suggests combined natural and sexual selection in an Amazonian fish. Biol J Linn Soc. 2019;127: 351–360. doi: 10.1093/biolinnean/blz054

60. Duponchelle F, Lino F, Hubert N, Panfili J, Renno JF, Baras E, et al. Environment-related life-history trait variations of the red-bellied piranha Pygocentrus nattereri in two river basins of the Bolivian Amazon. J Fish Biol. 2007;71: 1113–1134. doi: 10.1111/j.1095-8649.2007.01583.x

61. Mérona B, Mol J, Vigouroux R, Chaves P de T. Phenotypic plasticity in fish life-history traits in two neotropical reservoirs: Petit-saut reservoir in french guiana and brokopondo reservoir in suriname. Neotrop Ichthyol. 2009;7: 683–692. doi: 10.1590/S1679-62252009000400018

62. Basolo AL. Female preference for male sword length in the green swordtail, Xiphophorus helleri (Pisces: Poeciliidae). Anim Behav. 1990; doi: 10.1016/S0003-3472(05)80928–5

63. Walling CA, Royle NJ, Lindström J, Metcalfe NB. Do female association preferences predict the likelihood of reproduction? Behav Ecol Sociobiol. 2010;64: 541–548. doi: 10.1007/s00265-009-0869-4

64. Lochmatter T, Roduit P, Cianci C, Correll N, Jacot J, Martinoli A. Swistrack-a flexible open source tracking software for multi-agent systems. 2008 IEEE/RSJ International Conference on Intelligent Robots and Systems. 2008. pp. 4004–4010. Available: http://ieeexplore.ieee.org/xpls/abs_all.jsp?arnumber=4650937%5Cnpapers2://publication/uuid/ACAB96BB-2690-4469-AE61-81BBA79ACC56

65. R Core team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. 2018. Available: https://www.r-project.org/

66. Wong BBM, Candolin U. How is female mate choice affected by male competition? Biol Rev. 2005;80: 559–571. doi: 10.1017/S1464793105006809 16221329

67. Kidd MR, O’Connell LA, Kidd CE, Chen CW, Fontenot MR, Williams SJ, et al. Female preference for males depends on reproductive physiology in the African cichlid fish Astatotilapia burtoni. Gen Comp Endocrinol. 2013;180: 56–63. doi: 10.1016/j.ygcen.2012.10.014 23168085

68. Dougherty LR, Shuker DM. The effect of experimental design on the measurement of mate choice: a meta-analysis. Behav Ecol. 2015;26: 311–319. doi: 10.1093/beheco/aru125

69. Gabor C. Association patterns of sailfin mollies (Poecilia latipinna): Alternative hypotheses. Behav Ecol Sociobiol. 1999;46: 333–340. doi: 10.1007/s002650050627

70. Wagner WE. Measuring female mating preferences. Anim Behav. 1998;55: 1029–1042. doi: 10.1006/anbe.1997.0635 9632487

71. Stefanelli-Silva G, Zuanon J, Pires T. Revisiting Amazonian water types: Experimental evidence highlights the importance of forest stream hydrochemistry in shaping adaptation in a fish species. Hydrobiologia. 2019;830: 151–160. doi: 10.1007/s10750-018-3860-0

72. Dechaume-Moncharmont F-X, Freychet M, Motreuil S, Cézilly F. Female mate choice in convict cichlids is transitive and consistent with a self-referent directional preference. Front Zool. 2013;10: 69. doi: 10.1186/1742-9994-10-69 24216003

73. Dechaume-Moncharmont FX, Cornuau JH, Keddar I, Ihle M, Motreuil S, Cézilly F. Rapid assessment of female preference for male size predicts subsequent choice of spawning partner in a socially monogamous cichlid fish. Comptes Rendus—Biol. 2011;334: 906–910. doi: 10.1016/j.crvi.2011.08.004 22123092

74. Qvarnström A, Forsgren E. Should females prefer dominant males? Trends Ecol Evol. 1998;13: 498–501. doi: 10.1016/S0169-5347(98)01513-4 21238407

75. Andersson M. Female choice selects for extreme tail length in a widowbird. Nature. 1982;299: 818–820. doi: 10.1038/299818a0

76. Bischoff RJ, Gould JL, Rubenstein DI. Tail size and female choice in the guppy (Poecilia reticulata). Behav Ecol Sociobiol. 1985;17: 253–255. doi: 10.1007/BF00300143

77. Baldauf SA, Bakker TCM, Kullmann H, Thünken T. Female nuptial coloration and its adaptive significance in a mutual mate choice system. Behav Ecol. 2011; doi: 10.1093/beheco/arq226

78. Rosvall KA. Intrasexual competition in females: Evidence for sexual selection? Behavioral Ecology. 2011. pp. 1131–1140. doi: 10.1093/beheco/arr106 22479137

79. Freyhof J. Beobachtung bei der Zucht des Prachtsalmers Crenuchus spilurus Günther, 1863. Die Aquarien und Terr Zeitschrift. 1988;41: 209–211.

80. Amundsen T. Why are female birds ornamented? Trends Ecol Evol. 2000;15: 149–155. doi: 10.1016/s0169-5347(99)01800-5 10717684

81. Lindstrom K. The evolution of filial cannibalism and female mate choice strategies as resolutions to sexual conflict in fishes. Evolution (NY). 2000;54: 617–627.

82. FitzGerald GJ. Filial cannibalism in fishes: Why do parents eat their offspring? Trends Ecol Evol. 1992;7: 7–10. doi: 10.1016/0169-5347(92)90190-M 21235935

83. Manica A. Alternative strategies for a father with a small brood: Mate, cannibalise or care. Behav Ecol Sociobiol. 2002;51: 319–323. doi: 10.1007/s00265-001-0444-0

84. Petersen CW, Marchetti K. Filial cannibalism in the Cortez damselfish Stegastes rectifraenum. Evolution (NY). 1989;43: 158–168. doi: 10.1111/j.1558-5646.1989.tb04214.x 28568498

85. Forsgren E. Predation risk affects mate choice in a Gobiid fish. Am Nat. 1992;140: 1041–1049. doi: 10.1086/285455

86. Rosenthal GG, Wagner WE, Ryan MJ. Secondary reduction of preference for the sword ornament in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Anim Behav. 2002;63: 37–45. doi: 10.1006/anbe.2001.1887

Someone like me: Size-assortative pairing and mating in an Amazonian fish, sailfin tetra Crenuchus spilurus

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií