Wild populations are continuously challenged by natural environmental variation as well as threatened by anthropogenically-induced habitat loss and fragmentation. Non-genetic parental effects may be a key mechanism across taxa to cope with such environmental challenges and threats. However, the way in which environmental change modulates parental and offspring traits remains poorly studied in marine fish, especially in the wild. We empirically test whether environmental change directly affects monthly reproductive output and offspring phenotypes, including egg size, larval size and larval swimming abilities, in a wild population of anemonefish. In addition, we test whether environmentally induced parental physiology (hormones) modify parental traits, as well as offspring traits intergenerationally. First, we demonstrate plasticity in parental reproductive output when habitat size (anemone surface area) was experimentally manipulated. Second, we show intergenerational plasticity in wild anemonefish offspring traits. When habitat size increased, offspring traits were unchanged, but reproductive output was increased. Maternal reproductive hormones, such as 17ß-estradiol, showed a trend to increase when habitat size increased and 17ß-estradiol correlates positively with reproductive output. When habitat size decreased, reproductive output decreased, and smaller eggs and larvae were produced, however, these larvae swam faster. Our results provide evidence for marine fish plasticity in both reproductive output and offspring traits. In addition, the maternal reproductive hormone 17ß-estradiol plays a role in determining reproductive output and larval phenotypic traits. Through our study conducted in the wild, we show how changes in habitat size affect fitness of both parents and offspring in different ways. We highlight how parental and offspring plasticity, via intergenerational maternal effects, may ensure population persistence under environmental change.
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