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.

Effect of the administration of prolactin‐releasing peptide2 on feeding activity in the intertidal blenny Rhabdoblennius nitidus (Günther, 1861)

“…After spawning, males guard and aerate the eggs until hatching (6-7 days) (Miyano et al, 2006;Sano et al, 2019), during which time they can feed outside of the nests. However, some or all eggs are sometimes eaten by caregiving males (Matsumoto et al, 2011(Matsumoto et al, , 2018Takegaki et al, 2011). Both males and females reproduce several times in a breeding season, during which males repeat courtship and parental phases according to androgen-mediated brood cycling (Matsumoto et al, 2012(Matsumoto et al, , 2018.…”

Reproductive Strategies: Eat Your Kids to Restart Your Sex Life

“…In this issue of Current Biology, Matsumoto and colleagues [9] suggest that filial cannibalism may primarily serve to trigger a behavioral return to bachelor ways. In barred-chin blennies, adult male behavior cycles between a 'mating phase' when males are courting females and a 'parental phase' when they are guarding their young.…”

“…In female mammals, termination of parental care speeds a return to the reproductive state [2]. Similarly, Matsumoto et al [9] argue that filial cannibalism accomplishes an ''endocrinological reset'' -in this case, a return of androgen titers and courtship efforts to levels observed during the mating phase. When stuck with an unprofitable clutch, males eat their offspring to restart courtship.…”

“…By adding and removing eggs from nests in the wild, Matsumoto and colleagues [9] show that the presence or absence of eggs acts to rapidly modulate androgen levels and therefore courtship. Males with eggs in the nest have low androgen levels and infrequently perform courtship behaviors; but androgen and courtship levels rise dramatically after egg removal, with most males remating by the following day.…”

“…Selection also should favor females that can anticipate the probability of clutch destruction. While early studies suggested that females could use courtship vigor as a reliable cue of male nutritional state, and therefore risk of cannibalism [18], Matsumoto et al's work [9] suggests that vigorous courtship may, if anything, signal a male who's recently devoured his progeny. The importance of clutch size for male decisions suggests a tough choice for females: perhaps they maximize clutch survival by entrusting most of their reproductive output to one male, rather than hedging their bets across fathers [19].…”