Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets

Abstract

Multigenerational exposure is needed to assess the evolutionary potential of organisms in the rapidly changing seascape. Here, we investigate if there is a transgenerational effect of ocean acidification exposure on a calyptraeid gastropod such that long‐term exposure elevates offspring resilience. Larvae from wild type Crepidula onyx adults were reared from hatching until sexual maturity for over 36 months under three pH conditions (pH 7.3, 7.7, and 8.0). While the survivorship, growth, and respiration rate of F1 larvae were unaffected by acute ocean acidification (OA), long‐term and whole life cycle exposure significantly compromised adult survivorship, growth, and reproductive output of the slipper limpets. When kept under low pH throughout their life cycle, only 6% of the F1 slipper limpets survived pH 7.3 conditions after ~2.5 years and the number of larvae they released was ~10% of those released by the control. However, the F2 progeny from adults kept under the long‐term low pH condition hatched at a comparable size to those in medium and control pH conditions. More importantly, these F2 progeny from low pH adults outperformed F2 slipper limpets from control conditions; they had higher larval survivorship and growth, and reduced respiration rate across pH conditions, even at the extreme low pH of 7.0. The intragenerational negative consequences of OA during long‐term acclimation highlights potential carryover effects and ontogenetic shifts in stress vulnerability, especially prior to and during reproduction. Yet, the presence of a transgenerational effect implies that this slipper limpet, which has been widely introduced along the West Pacific coasts, has the potential to adapt to rapid acidification.

Ocean acidification does not overlook sex: Review of understudied effects and implications of low pH on marine invertebrate sexual reproduction

“…One study found that OA can increase fecundity, and another found that low pH increased reproductive output, but at the cost of body size and shell integrity (Fitzer et al, 2012b;Engström-Öst et al, 2014). In molluscs, OA exposure during breeding reduced bivalve brood size (Wippel, 2017;Maboloc and Chan, 2021), while a previous OA exposure resulted in increased brood size but no effect to overall larval production (Spencer et al, 2020). Instances where reproductive output increases may be a short-term stress response or may indicate adaptive potential to pH change (Engström-Öst et al, 2014).…”

Effects of high pCO2on snow crab larvae: Carryover effects from embryogenesis and oogenesis reduce direct effects on larval survival

“…It could be selection, through selective mortality of females poorly adapted to low pH, or transgenerational plasticity [22]. Transgenerational and selective breeding experiments suggest that many species have the capacity to evolutionarily adapt to ocean acidification via natural selection [26,[53][54][55][56]. In the case of snow crabs, the mortality over the course of the experiment did not vary much between the treatments which makes this a less likely, though still possible, mechanism [57].…”

Paternal hypoxia exposure primes offspring for increased hypoxia resistance

“…These studies suggest that parents can transmit information that may benefit offspring survival. Through this transgenerational plasticity (also known as transgenerational acclimation [16][17][18]), parents may provide offspring with increased tolerance to environmental perturbations, such as contaminants [1][2][3][4][5], food shortages [19,20], carbon dioxide [21][22][23][24], hypoxia [25], salinity [26][27][28], and temperature [20,[29][30][31][32][33][34][35]. Studies have tended to focus on maternal transgenerational plasticity, or have exposed both parents to the environmental perturbation, making it impossible to disentangle the relative roles of mothers and fathers in altering offspring phenotype [36,37].…”