Reproductive effort and terminal investment in a multi-species assemblage of Amazon electric fish

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
(B. beebei) exhibits a two-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.