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Filial Cannibalism by Male Fish as an Infanticide to Restart Courtship by Self-Regulating Androgen Levels

2018; Elsevier BV; Volume: 28; Issue: 17 Linguagem: Inglês

10.1016/j.cub.2018.06.056

1879-0445

Yukio Matsumoto, Tetsunari Tateishi, Ryusuke Terada, Kiyoshi Soyano, Takeshi Takegaki,

Marine and fisheries research

Parental care is costly for animal parents [1Clutton-Brock T.H. The Evolution of Parental Care. Princeton University Press, 1991Crossref Google Scholar, 2Smith C. Wootton R.J. The costs of parental care in teleost fishes.Rev. Fish Biol. Fish. 1995; 5: 7-22Crossref Scopus (160) Google Scholar, 3Alonso-Alvarez C. Velando A. Benefits and costs of parental care.in: Royle N.J. Smiseth P.T. Kolliker M. The Evolution of Parental Care. Oxford University Press, 2012: 40-60Crossref Google Scholar], who often desert, abort, or kill their offspring and sometimes even eat them—so-called filial cannibalism [1Clutton-Brock T.H. The Evolution of Parental Care. Princeton University Press, 1991Crossref Google Scholar, 4Elgar M.A. Crespi B.J. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford University Press, 1992Google Scholar]. A primary adaptive hypothesis for filial cannibalism centers on the expected nutritional benefits from eating offspring (the energy-based [EB] hypothesis [5Rohwer S. Parent cannibalism of offspring and egg raiding as a courtship strategy.Am. Nat. 1978; 112: 429-440Crossref Google Scholar, 6Sargent R.C. Ecology of filial cannibalism in fish: theoretical perspectives.in: Elgar M.A. Crespi B.J. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford University Press, 1992: 38-62Google Scholar, 7Sargent R.C. Crowley P.H. Huang C. Lauer M. Neergaard D. Schmoetzer L. A dynamic program for male parental care in fishes: brood cycling and filial cannibalism.Behaviour. 1995; 132: 1059-1078Crossref Scopus (26) Google Scholar]). However, many empirical studies are inconsistent with the EB hypothesis [8Manica A. Filial cannibalism in teleost fish.Biol. Rev. Camb. Philos. Soc. 2002; 77: 261-277Crossref PubMed Scopus (199) Google Scholar, 9Klug H. Bonsall M.B. When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism.Am. Nat. 2007; 170: 886-901Crossref PubMed Scopus (88) Google Scholar]. One notable case is total filial cannibalism observed in some fishes. The caregiving males of these species eat all eggs and restart reproduction when tending a small number of eggs, as predicted by the EB hypothesis; but, this is puzzling because they can potentially court females even while tending eggs and increase the eggs by additional matings. Here we show that brood termination known as total filial cannibalism in blenniid fish Rhabdoblennius nitidus males is an endocrinological necessity to restart courtship behavior for subsequent mating. Males exhibit androgen-dependent brood cycling, and they are normally incapable of exhibiting courtships during the parental phase [10Matsumoto Y. Yabuno A. Kiros S. Soyano K. Takegaki T. Changes in male courtship intensity and androgen levels during brood cycling in the blenniid fish Rhabdoblennius nitidus.J. Ethol. 2012; 30: 387-394Crossref Scopus (9) Google Scholar]. Egg manipulation experiments demonstrated that egg presence in the nest is a key stimulus regulating male androgen levels; they cannot restart courtship until removing all eggs. Furthermore, surprisingly, eggs were sometimes spit out without being consumed, and the occurrence of cannibalization and removal of all eggs was not associated with male condition. These results strongly suggest that the egg cannibalistic and removal behaviors that have been regarded as total filial cannibalism in this species are infanticide or embryocide rather than cannibalism, which serve to increase the males’ androgen levels.