Maternal investment mediates offspring life history variation with context‐dependent fitness consequences

Abstract

Maternal effects, such as per capita maternal investment, often interact with environmental conditions to strongly affect traits expressed early in ontogeny. However, their impact on adult life history traits and fitness components is relatively unknown. Theory predicts that lower per capita maternal investment will have strong fitness costs when the offspring develop in unfavorable conditions, yet few studies have experimentally manipulated per capita maternal investment and followed offspring through adulthood. We used a surgical embryonic yolk removal technique to investigate how per capita maternal investment interacted with an important ecological factor, larval density, to mediate offspring life history traits through reproductive maturity in an amphibian, Ambystoma talpoideum. We predicted that increased larval density would reinforce the life history variation induced by differences in per capita investment (i.e., Controls vs. Reduced Yolk), with Reduced larvae ultimately expressing traits associated with lower fitness than Controls when raised at high densities. We found that Reduced individuals were initially smaller and more developed, caught up in size to Controls within the first month of the larval stage, but were smaller at the end of the larval stage in low densities. Reduced individuals also were more likely to undergo metamorphosis at high densities and mature 'females invested in more eggs for their body sizes than Controls. Together, our results do not support our hypothesis, but instead indicate that Reduced individuals express traits associated with higher fitness when they develop in high-density environments, but lower fitness in low-density environments. The observed life history and fitness patterns are consistent with the "maternal match" hypothesis, which predicts that when the maternal environment (e.g., high density) results in phenotypic variation that is transmitted to the offspring (e.g., reduced per capita yolk investment), and offspring face that same environment (e.g., high larval density), the fitness of both mother and offspring is maximized.

The effects of embryonic experience with predation risk vary across a wave exposure gradient

“…These results support our hypothesis that because green crab abundance is lower and likely more variable on wave-exposed shores, wave-exposed snails display greater plasticity in response to predation risk, as well as the results of our previous work showing that embryonic experience with risk causes wave-exposed snails to emerge at a smaller size (Donelan and Trussell 2018a). Emerging at a smaller size, however, is likely maladaptive (but see Moore et al 2015) because it can reduce an individual's energetic stores (Rivero and West 2002), increase vulnerability to predators (Janzen et al 2001), and delay reproduction (Marshall et al 2003). The fact that wave-exposed, but not sheltered, snails incur these fitness costs suggests that sensitivity to predation risk during development is favored only in environments where uncertainty about risk is high (i.e., wave-exposed shores).…”

“…Emerging at a smaller size, however, is likely maladaptive (but see Moore et al. ) because it can reduce an individual's energetic stores (Rivero and West ), increase vulnerability to predators (Janzen et al. ), and delay reproduction (Marshall et al.…”

A mother’s legacy: the strength of maternal effects in animal populations

“…It is also intriguing that maternal effects influence adult traits as greatly as they do juvenile traits for physiology and behaviour, as well as in species without prolonged maternal care. In this broad range of conditions, adult selective pressures may therefore be an overlooked factor shaping the evolutionary significance of maternal effects (see also Coulson et al ; Warner & Shine ; Marshall & Monro ; Moore et al ).…”

The predictability and magnitude of life‐history divergence to ecological agents of selection: a meta‐analysis in livebearing fishes

“…In such cases, offspring receiving seemingly suboptimal investment may not only survive, but may eventually minimise fitness differences through mechanisms such as compensatory growth and reproduction (e.g. Lindholm et al 2006;Moore et al 2015; but see Auer et al 2010). Such patterns may mitigate the strength of selection on investment in offspring size, for example, and may lead to the evolution of multiple, optimal life-history strategies across populations or species (Wilbur et al 1974;Losos 2011).…”