Life histories of closely related amphidromous and non‐migratory fish species: a trade‐off between egg size and fecundity

Abstract

Summary Amphidromy is a widespread migratory behavioural syndrome exhibited by fish (and some aquatic invertebrates) that spawn in fresh water and whose larvae migrate to pelagic marine (or lentic) habitats for a period of early growth, followed by a return migration to adult freshwater habitats. The fitness advantage of amphidromy has been the subject of prolonged debate, and we examined the hypothesis that amphidromy mainly increases fecundity through the production of small pelagic larvae. We compared egg size (a proxy for larval size) of closely related non‐migratory and amphidromous fish species in the families Cottidae, Galaxiidae, Eleotridae and Gobiidae. To examine how egg size changes in relation to body size within a taxonomic group, we also compared egg size and maximum body size across most species of New Zealand non‐migratory and amphidromous galaxiids. Non‐migratory species generally have relatively larger eggs than their amphidromous confamilial species. This particular trait has evolved independently several times in each of the four families of amphidromous fish that have given rise to significant freshwater radiations. Amongst the New Zealand galaxiids, mean egg diameter increased with maximum body length for both non‐migratory and amphidromous species; however, despite the considerably smaller relative body size of the non‐diadromous species, the rate of increase in egg diameter relative to the increase in body size is considerably higher in the non‐migratory fish. We propose that amphidromous fish maintain a high level of fecundity by producing small pelagic larvae. In contrast, the relatively large eggs and well‐developed larvae of non‐migratory species increase larval survival in what are often relatively harsh and unproductive freshwater habitats. Consequently, amphidromous species are likely to have a competitive advantage over their non‐migratory relatives when close to a pelagic habitat in which their larvae can grow and develop and then migrate upstream, releasing them from recruitment limitation and giving them a local reproductive advantage over their less fecund non‐migratory relatives. We argue that the persistence and distribution of both life‐history strategies across the landscape depends on the relative difference in the net reproductive return for each strategy in relation to distance from a pelagic larval habitat, as mediated by the relative costs of migration and egg size/fecundity relationships.

The positive correlation between maternal size and offspring size: fitting pieces of a life‐history puzzle

“…First, the maternal-size correlation appears to be observed in nearly all plant and animal taxa (Roff, 2002;Lim et al, 2014). 3), the qualitative pattern of the maternal-size correlation is similar both within and among species (Blueweiss et al, 1978;Visman et al, 1996;Roff, 2002), across modes of migration (Tamate & Maekawa, 2000;Acolas et al, 2008;Closs, Hicks & Jellyman, 2013), and across modes of parity (Heath & Blouw, 1998;Crespi & Teo, 2002). Third, as we emphasize below (Fig.…”

“…In experimental studies, it is clear that increased offspring density can decrease w in some cases (Wall & Begon, 1986;Marshall, Cook & Emlet, 2006), and it is clear that relatively large offspring tend to fare better under competition (Stanton, 1984;Hutchings, 1991;Bashey, 2008; but see McIntyre & Gooding, 2000). ), each data point is a unique species [redrawn from Closs et al (2013)]. (C) Across 12 species of galaxiids (Galaxias spp.…”

Interspecific differences in early life‐history traits in a species complex of stream‐resident galaxiids

“…The G. vulgaris complex is descended from a common amphidromous ancestor (Waters et al 2010). A loss of amphidromy is associated with an increase in egg and larval size, which allows nonmigratory species to complete their life cycles in low productivity freshwater habitats (Goto 1990;Closs et al 2013). The interspecific differences seen here suggest that colonisation of high altitude headwater creeks requires a continuation of this evolutionary process.…”

“…A balance must be struck between overprovisioning eggs, which could potentially reduce fecundity below that required to counter mortality rates, and under-provisioning, which could render offspring unfit to survive the environmental conditions encountered. Optimal offspring size can vary in relation to food availability in the rearing environment (Goto 1990;Hutchings 1991;Einum & Fleming 1999;Closs et al 2013). Life-history theory would suggest the optimal balance in this trade-off is to sufficiently provision offspring to make survival likely, but allocate any additional resources to maximise the number of recruits (Hutchings 1991;Einum & Fleming 1999, 2000Einum 2003;Rollinson & Hutchings 2013).…”

A Preliminary Transcriptomic Study of Galaxiid Fishes Reveals a Larval Glycoprotein Gene Under Strong Positive Selection

“…These experiments are confounded by a difference in timing of development between diadromous G. argenteus and nondiadromous G. depressiceps, the former (more r-selected) species hatching at an earlier developmental stage. Therefore, although diadromous species eggs are less well-provisioned (Closs et al 2013), the yolk sac is actually larger at the time of hatching. depressiceps sense depressiceps anti-sense argenteus anti-sense argenteus sense Fig.…”