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

Abstract

Parental care is costly for animal parents [1-3], who often desert, abort, or kill their offspring and sometimes even eat them-so-called filial cannibalism [1,4]. A primary adaptive hypothesis for filial cannibalism centers on the expected nutritional benefits from eating offspring (the energy-based [EB] hypothesis [5-7]). However, many empirical studies are inconsistent with the EB hypothesis [8, 9]. 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 [10]. 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.