Heatwave-mediated maternal effects: heat stress in late but not early pregnancy has carry over effects on offspring phenotype

Chiara Morosinotto , Merel C. Breedveld, Alessandra Stevanato, Nadia Zanelli, Alessandro Devigili, Clelia Gasparini

Heatwaves are extreme climatic events driven by climate change that profoundly affect animal survival and reproduction. Although evidence for the direct effects of heatwaves on reproduction is increasing, much less is known about whether heatwaves during pregnancy generate maternal effects on offspring, and whether these effects depend on the timing of exposure. Pregnancy is a metabolically demanding life-history phase, with energetic demands changing markedly across gestation. We experimentally exposed pregnant female guppies (Poecilia reticulata), a small viviparous tropical fish, to a five-day simulated heatwave during either early or late pregnancy. We quantified maternal reproductive success and offspring performance, behaviour and sexually selected traits. Brood size did not differ across groups, but maternal heat exposure in late pregnancy was associated with body size-dependent effects on within-brood mortality; larger females exposed to heat late in pregnancy were more likely to experience offspring mortality. Despite no detectable effects on offspring growth, late gestational heatwaves altered offspring behaviour and adult offspring phenotype. Offspring of late-exposed mothers exhibited increased exploratory behaviour and swimming velocity measured in an open field assay, whereas overall swimming performance was unaffected, suggesting that these behavioural differences were not explained by altered swimming capacity. Maternal heat exposure also altered the degree of within-treatment variability in some phenotypic traits, suggesting that heatwaves may influence not only mean offspring phenotype but also degree of phenotypic variation. Moreover, adult male offspring (F1) from late-exposed mothers displayed a greater extent of orange body coloration, a key sexually selected trait in guppies, whereas sperm traits were unaffected in all descendant males. Overall, our findings demonstrate that heatwaves during gestation, and especially during its late stages, can alter females’ reproductive success and shape the development of offspring behavioural and sexually-selected traits via maternal effects. The developmental timing of maternal heat exposure is a decisive factor determining the magnitude and nature of maternal effects, with consequences that persist until sexual maturity. By influencing exploration and sexual traits, heatwave-mediated maternal effects may alter offspring fitness and population responses to increasingly frequent climatic extremes, and may produce cross-generational effects extending beyond directly exposed individuals.