Male mating tactics and secondary sexual traits: insights from the Mediterranean killifish, Aphanius fasciatus
Luca Altavilla A B * , Chiara Facca A , Francesco Cavraro A , Mirko Liuzzo A and Stefano Malavasi AA
B
Abstract
Sexual selection results from male competition and female choice linked by complex interactions that drive the population’s life history, often leading to the development of specific secondary sexual traits with an increased reproductive success.
To investigate the male mating tactics and the role of a secondary sexual trait (‘black band’ on the caudal fin) along the male ontogenetic development in the Mediterranean killifish, Aphanius fasciatus (Valenciennes, 1821).
Male–male competition was investigated through a combination of an extensive field collection and behavioural analysis under controlled conditions, comparing four groups differing in the presence or absence of the black band and body size.
Banded males courted more and tended to monopolise the female, but the overall spawning performance did not differ significantly among the analysed groups.
(1) The black band on the caudal fin depends on ontogeny; (2) all mature males express the entire courtship and competitive repertory; (3) sexual maturity occurs in fish of at least 20 mm; (4) large size and presence of the black band seem to contribute to male dominance.
This study has highlighted the role of Aphanius fasciatus as an excellent model for studying polygynandrous mating systems, on the basis of intense male–male competition.
Keywords: Aphanius fasciatus, Cyprinodontidae, fish behaviour, killifish, male–male competition, mating behaviour, secondary sexual traits, sexual selection.
References
Almasi B, Roulin A, Jenni-Eiermann S, Jenni L (2008) Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in barn owls. Hormones and Behavior 54(1), 217-223.
| Crossref | Google Scholar |
Archard GA, Braithwaite VA (2011) Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: population and sex differences. Behavioural Processes 86(1), 52-57.
| Crossref | Google Scholar |
Barlow GW (1961) Social behavior of the desert pupfish, Cyprinodon macularius, in the field and in the aquarium. The American Midland Naturalist 65(2), 339-359.
| Google Scholar |
Brantley RK, Wingfield JC, Bass AH (1993) Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Hormones and Behavior 27(3), 332-347.
| Crossref | Google Scholar | PubMed |
Cavraro F, Torricelli P, Malavasi S (2013) Quantitative ethogram of male reproductive behavior in the South European toothcarp Aphanius fasciatus. The Biological Bulletin 225(2), 71-78.
| Crossref | Google Scholar |
Cavraro F, Varin C, Malavasi S (2014) Lunar-induced reproductive patterns in transitional habitats: insights from a Mediterranean killifish inhabiting northern Adriatic saltmarshes. Estuarine, Coastal and Shelf Science 139, 60-66.
| Crossref | Google Scholar |
Cavraro F, Gheno G, Ganzerla R, Zucchetta M, Franzoi P, Malavasi S (2018) Habitat constraints on carotenoid-based coloration in a small euryhaline teleost. Ecology and Evolution 8(9), 4422-4430.
| Crossref | Google Scholar |
Cavraro F, Finotti G, Rossato G, Zucchetta M, Facca C, Malavasi S (2021) A comparative analysis of habitat quality between artificial and natural creeks in the Mediterranean killifish Aphanius fasciatus: implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 31(6), 1311-1321.
| Crossref | Google Scholar |
Doutrelant C, McGregor PK (2000) Eavesdropping and mate choice in female fighting fish. Behaviour 137(12), 1655-1669 Available at http://www.jstor.org/stable/4535799.
| Google Scholar |
Evans MR, Norris K (1996) The importance of carotenoids in signaling during aggressive interactions between male firemouth cichlids (Cichlasoma meeki). Behavioral Ecology 7(1), 1-6.
| Crossref | Google Scholar |
Facca C, Cavraro F, Franzoi P, Malavasi S (2020) Lagoon resident fish species of conservation interest according to the Habitat Directive (92/43/CEE): a review on their potential use as ecological indicator species. Water 12(7), 2056.
| Crossref | Google Scholar |
Frischknecht M (1993) The breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigour. Evolutionary Ecology 7(5), 439-450.
| Crossref | Google Scholar |
Fuller RC (2001) Patterns in male breeding behaviors in the bluefin killifish, Lucania goodei: a field study (Cyprinodontiformes: Fundulidae). Copeia 2001(3), 823-828.
| Crossref | Google Scholar |
Grech M, Schembri PJ (1993) Observations on courtship and mating behaviour in maltese populations of the killifish Apnonius fasciatus (Pisces: Cyprinodontidae). The Central Mediterranean Naturalist 2(2), 28-34.
| Google Scholar |
Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54(5), 1712-1724.
| Crossref | Google Scholar | PubMed |
Gunderson DR (1997) Trade-off between reproductive effort and adult survival in oviparous and viviparous fishes. Canadian Journal of Fisheries and Aquatic Sciences 54(5), 990-998.
| Crossref | Google Scholar |
Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proceedings of the Royal Society of London – B. Biological Sciences 270(1519), 1033-1040.
| Crossref | Google Scholar |
Houde AE (1987) Mate choice based upon naturally occurring color-pattern variation in a guppy population. Evolution 41(1), 1-10.
| Crossref | Google Scholar |
Johnson AM, Fuller RC (2015) The meaning of melanin, carotenoid, and pterin pigments in the bluefin killifish, Lucania goodei. Behavioral Ecology 26(1), 158-167.
| Crossref | Google Scholar |
Kodric-Brown A (1985) Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology 17(3), 199-205.
| Crossref | Google Scholar |
Kodric-Brown A (1986) Satellites and sneakers: opportunistic male breeding tactics in pupfish (Cyprinodon pecosensis). Behavioral Ecology and Sociobiology 19(6), 425-432.
| Crossref | Google Scholar |
Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behavioral Ecology and Sociobiology 25(6), 393-401.
| Crossref | Google Scholar |
Kodric-Brown A (1990) Mechanisms of sexual selection: insights from fishes. Annales Zoologici Fennici 27(2), 87-100.
| Google Scholar |
Kodric-Brown A (1998) Sexual dichromatism and temporary color changes in the reproduction of fishes. American Zoologist 38(1), 70-81.
| Crossref | Google Scholar |
Kodric-Brown A, Nicoletto PF (1993) The relationship between physical condition and social status in pupfish Cyprinodon pecosensis. Animal Behaviour 46(6), 1234-1236.
| Crossref | Google Scholar |
Leiser JK, Itzkowitz M (2002) The relative costs and benefits of territorial defense and the two conditional male mating tactics in the Comanche Springs pupfish (Cyprinodon elegans). Acta Ethologica 5(1), 65-72.
| Crossref | Google Scholar |
Leiser JK, Itzkowitz M (2004) Changing tactics: dominance, territoriality, and the responses of ‘primary’ males to competition from conditional breeders in the variegated pupfish (Cyprinodon variegatus). Behavioural Processes 66(2), 119-130.
| Crossref | Google Scholar |
Leonardos I (2008) The feeding ecology of Aphanius fasciatus (Valenciennes, 1821) in the lagoonal system of Messolongi (western Greece). Scientia Marina 72(2), 393-401.
| Google Scholar |
Leonardos I, Sinis A (1998) Reproductive strategy of Aphanius fasciatus Nardo, 1827 (Pisces: Cyprinodontidae) in the mesolongi and etolikon lagoons (W. Greece). Fisheries Research 35(3), 171-181.
| Crossref | Google Scholar |
Lott DF (1979) Dominance relations and breeding rate in mature male American bison. Zeitschrift Für Tierpsychologie 49(4), 418-432.
| Crossref | Google Scholar |
Mafli A, Wakamatsu K, Roulin A (2011) Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises. Animal Behaviour 81(4), 859-863.
| Crossref | Google Scholar |
Malavasi S, Georgalas V, Cavraro F, Torricelli P (2010) Relationships between relative size of sexual traits and male mating success in the Mediterranean killifish Aphanius fasciatus (Nardo, 1827). Marine and Freshwater Behaviour and Physiology 43(3), 157-167.
| Crossref | Google Scholar |
Maltagliati F (2002) Genetic monitoring of brackish-water populations: the Mediterranean toothcarp Aphanius fasciatus (Cyprinodontidae) as a model. Marine Ecology Progress Series 235(1988), 257-262.
| Crossref | Google Scholar |
Mayer I, Borg B, Schulz R (1990) Seasonal changes in and effect of castration/androgen replacement on the plasma levels of five androgens in the male three-spined stickleback, Gasterosteus aculeatus L. General and Comparative Endocrinology 79(1), 23-30.
| Crossref | Google Scholar |
McGhee KE, Fuller RC, Travis J (2007) Male competition and female choice interact to determine mating success in the bluefin killifish. Behavioral Ecology 18(5), 822-830.
| Crossref | Google Scholar |
Paterson AW, Whitfield AK (2000) Do shallow-water habitats function as refugia for juvenile fishes? Estuarine, Coastal and Shelf Science 51(3), 359-364.
| Crossref | Google Scholar |
Pizzolon M, Rasotto MB, Mazzoldi C (2008) Male lagoon gobies, Knipowitschia panizzae, prefer more ornamented to larger females. Behavioral Ecology and Sociobiology 62(4), 521-528.
| Crossref | Google Scholar |
Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5(4), 297-307.
| Crossref | Google Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675.
| Crossref | Google Scholar |
Sowersby W, Eckerström-Liedholm S, Rowiński PK, Balogh J, Eiler S, Upstone JD, Gonzalez-Voyer A, Rogell B (2022) The relative effects of pace of life-history and habitat characteristics on the evolution of sexual ornaments: a comparative assessment. Evolution 76(1), 114-127.
| Crossref | Google Scholar |
Taborsky M (2001) The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. Journal of Heredity 92(2), 100-110.
| Crossref | Google Scholar |
Triantafyllidis A, Leonardos I, Bista I, Kyriazis ID, Stoumboudi MT, Kappas I, Amat F, Abatzopoulos TJ (2007) Phylogeography and genetic structure of the Mediterranean killifish Aphanius fasciatus (Cyprinodontidae). Marine Biology 152(5), 1159-1167.
| Crossref | Google Scholar |