Reproductive effort and terminal investment in a multispecies assemblage of Amazon electric fish

Abstract

The terminal investment hypothesis (TIH) predicts that individuals with favorable prospects for future reproduction (i.e., high residual reproductive value, RRV) should moderate current reproductive investment in favor of growth, survival, and future reproduction, whereas those with low RRV should “terminally invest” by diverting somatic resources towards current reproduction at the expense of future reproduction. However, support for the TIH in wild animal populations is fragmentary, and the ecological contexts of terminal investment remain poorly known. We report a remarkable case of simultaneous terminal investment involving five sympatric species of the electric knifefish genus Brachyhypopomus, from Amazonian floodplain and terra firme stream habitats. We found that terminal investment is synchronized by seasonal breeding, in response to circannual environmental variation in mortality risk. Four species exhibit a uniseasonal iteroparous (annual) life history with complete post-reproductive mortality after a single breeding season. One species (Brachyhypopomus beebei) exhibits a 2-year multiseasonal iteroparous life history with breeding in two seasons and post-reproductive mortality after the second. In mature females and (most) males of the annual species, as well as in both mature female and male second-year (but not first-year) B. beebei, we documented an increase in two metrics of reproductive effort (size-adjusted gonad mass and electric signal amplitude) and a concomitant reduction in somatic condition (size-adjusted somatic mass), all in response to proximity to the end of the common breeding season, when RRV approximates zero. In mature first-year B. beebei, we documented neither an increase in reproductive effort nor a decline in somatic condition, implying an alternative strategy of reproductive restraint. Our findings support Kirkwood's disposable soma theory, which posits that death by reproductive exhaustion can be delayed if terminal investment is replaced by reproductive restraint, allowing individuals to survive and breed in a subsequent season. Deferral of the terminal investment response in annual species, and the origin of a gonadal regression-regeneration sequence, may open pathways for rapid evolutionary transitions to multiseasonal iteroparity. Excepting the age (year-group) dependency of terminal investment in B. beebei, we were unable to identify intrinsic cues or extrinsic environmental cues for the terminal investment response in Brachyhypopomus.