Visual preference of males for conspecific mates in mutually ornamented fish: possible support for the species recognition hypothesis
Because sexual selection typically acts on males, the evolution of conspicuous ornamentation in females has been insufficiently studied. Genetic correlation between the sexes and sexual or social selection on females have been proposed to explain female ornamentation, but they cannot fully explain certain patterns observed in nature such as female ornamentation in non-territorial, promiscuous species. The species recognition hypothesis, which postulates that ornamentation is adaptive because it prevents maladaptive hybridization, might plausibly explain female ornamentation. We examined this in two sympatric, non-territorial, promiscuous fish species, Tribolodon hakonensis (TH) and Tribolodon sachalinensis (TS), in which both sexes display species-specific conspicuous coloration in the breeding season. We conducted experiments on visual mate choice of male TH for conspecific and heterospecific females, and compared their association times. TH spent more time near conspecifics, indicating that they used visual cues to recognize them. Because the females of the two species presented to the males did not differ in body size, shape or behavior, male preference for conspecifics was probably based on female nuptial coloration. These results suggest that female ornamentation may evolve or be maintained not only by sexual or social selection within a species but also by interspecific interactions (e.g., hybridization).
KeywordsMale mate choice Sexual monomorphism Sexual isolation Breeding coloration Far Eastern daces
We are grateful to T. Ishii for tremendous help in setting up the experimental system, to M. Kudoh, K. Takahashi, T. Tsuruya, and K. Tomita for sampling assistance, and to all the staff of the Tomakomai Experimental Forest of Hokkaido University for their support of this research. We thank the three anonymous reviewers who provided constructive comments on the manuscript. We also thank M. Kikuchi and Salmon Hometown Chitose Aquarium for allowing us to conduct preliminary trials by computer animation, C. Ayer for checking the English of the manuscript, and Y. Ohkubo for advice on the statistical analyses.
K. A. designed the study and performed the experiments; O. K. contributed to the study design; K. A., O. K., and I. K. prepared the manuscript.
This study was supported by a Sasakawa Scientific Research Grant from the Japan Science Society, by the Fujiwara Natural History Foundation, by a grant-in-aid from the Japan Society for the Promotion of Science (JSPS) for a research fellow (18J10096) to K. A., and by a JSPS KAKENHI grant (17H03725) to O. K.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
Consent for publication
Formal approval for the experiment was granted by the Institutional Animal Care and Use Committee of Hokkaido University (approval no. 28-2). Sampling was approved by the local government of Hokkaido Prefecture.
- Amorim M (2006) Diversity of sound production in fish. In: Ladich F (ed) Communication in fishes. Science Publishers, Boca Raton, pp 71–105Google Scholar
- Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
- Atsumi K, Koizumi I (2017a) Early maturation of rosyface dace, Tribolodon sachalinensis (Cyprinidae, Cypriniformes), in a small isolated population. Biogeography 19:123–126Google Scholar
- Development Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Gavrenkov YI, Ivankov VN (1981) The taxonomic status and biology of the “Pacific Redfin” of the genus Tribolodon of the Southern Maritime Territory. J Ichthyol 19:47–56Google Scholar
- Gavrenkov YI, Kolpakov NV, Kolpakov EV (2004) Specific features of biology of Pacific Redfins of the genus Tribolodon (Cyprinidae) in waters off Northern Primorye. J Ichthyol 44:217–223Google Scholar
- Gillam E (2011) An introduction to animal communication. Nat Educ Knowl 3:70. https://doi.org/10.1093/acprof:oso/9780199677184.003.0001 Google Scholar
- Gritsenko OF (1982) Reproduction ecology of the eastern redfins of genus Tribolodon (Cyprinidae). J Ichthyol 22:121–134Google Scholar
- Hanzawa N, Taniguchi N, Shinzawa H (1984) Genetic markers of the artificial hybrids between Tribolodon hakonensis and T. sp. (Ukekuchi–ugui). Otsuchi Mar Res Cent Rep 10:11–17Google Scholar
- Härdling R, Kokko H (2005) The evolution of prudent choice. Evol Ecol Res 1:697–715Google Scholar
- Ito Y (1975) Notes on the spawning habits of three species of genus Tribolodon in Hokkaido. Sci Rep Hokkaido Fish Hatch 30:39–42Google Scholar
- Moriyama T, Fujisaku M, Mizutani M, Goto A (2008) Migration of Japanese dace (Ugui) in water zone network formed by streams, canal and river utilized for irrigation and drainage. Irrig Drain Rural Eng J 10:85–93Google Scholar
- Nakamura M (1969) Cyprinid fishes of Japan: studies on the life history of cyprinid fishes of Japan. Research Institute of Natural Resources, TokyoGoogle Scholar
- Rohlf F (2013) tpsDIG2: Digitize landmarks and outlines from image files, scanner, or video. http://life.bio.sunysb.edu/morph/soft–dataacq.html/. Accessed 12 June 2016
- Sabaj MH, Maurakis EG, Woolcott WS (2000) Spawning behaviors in the bluehead chub, Nocomis leptocephalus, river chub, N. micropogon and central stoneroller, Campostoma anomalum. Am Midl Nat 144:187–201. https://doi.org/10.1674/0003-0031(2000)144%5b0187:sbitbc%5d2.0.co;2 CrossRefGoogle Scholar
- Sakai H (1995) Life-histories and genetic divergence in three species of Tribolodon (Cyprinidae). Mem Fac Fish Hokkaido Univ 42:1–98Google Scholar
- Sakai H, Hamada K (1985) Electrophoretic discrimination of Tribolodon species (Cyprinidae) and the occurrence of their hybrids. Jpn J Ichthyol 32:216–224Google Scholar
- Sakai H, Saitoh T, Takeuchi M et al (2007) Cyprinid inter-generic hybridisation between Tribolodon sachalinensis and Rhynchocypris lagowskii in Tohoku district. J Nat Fish Univ 55:45–52Google Scholar
- Shine R, Reed RN, Shetty S et al (2002) Reproductive isolating mechanisms between two sympatric sibling species of sea snakes. Evolution 56:1655–1662. https://doi.org/10.1111/j.0014-3820.2002.tb01477.x CrossRefGoogle Scholar
- Sviridov VV, Ivankov VN, Luk’yanov PE (2002) Variation of breeding dress of eastern redfins of the genus Tribolodon. I. Tribolodon brandti and T. ezoe. J Ichthyol 42:558–563Google Scholar
- Sviridov VV, Ivankov VN, Luk’yanov PE (2003) Variability of breeding coloration in the genus Tribolodon. II. Tribolodon hakuensis. J Ichthyol 43:106–109Google Scholar
- von Schilcher F, Dow M (1977) Courtship behaviour in Drosophila: sexual isolation or sexual selection? Z Tierpsychol 43:304–310. https://doi.org/10.1111/j.1439-0310.1977.tb00077.x CrossRefGoogle Scholar
- Wallace AR (1889) Darwinism: an exposition of the theory of natural selection with some of its applications. Macmillan, LondonGoogle Scholar
- Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric morphometrics for biologists: a primer, 2nd edn. Academic Press, New YorkGoogle Scholar