Low pH Means More Female Offspring: A Multigenerational Plasticity in the Sex Ratio of Marine Bivalves

Abstract

Global changes can profoundly affect the sex determination and reproductive output of marine organisms, disrupting the population structure and ecosystems. High CO₂driven low pH in the context of ocean acidification (OA) has been shown to severely affect various calcifiers, but less is known about the extent to which low pH influences sex determination and reproduction of marine organisms, particularly mollusks. This study is the first to report a biased sex ratio over multiple generations toward females, driven by exposure to high CO₂-induced low pH environments, using the ecologically and economically important Portuguese oyster (Crassostrea angulata) as a model. This phenomenon, which we term pH-mediated sex determination (PSD), has no consequences for fecundity, gonadal development, or reproductive function in the offspring. Moreover, PSD persisted into a second year of reproduction and was inherited across multiple generations. Transcriptomic analysis indicates PSD is associated with the activation of the Wnt signaling pathway in females and inhibition of spermiogenesis-related functions in males. This work expands our understanding of environmental sex determination and highlights the possible impact of global changes on reproduction and population dynamics of mollusks and other marine organisms.