Faster juvenile growth promotes earlier sex change in a protandrous hermaphrodite (barramundi Lates calcarifer)

Abstract

The relationship between growth and sexual maturation is central to understanding the dynamics of animal populations which exhibit indeterminate growth. In sequential hermaphrodites, which undergo post-maturation sex change, the size and age at which sex change occurs directly affects reproductive output and hence population productivity. However, these traits are often labile, and may be strongly influenced by heterogenous growth and mortality rates. We analysed otolith microstructure of a protandrous (i.e., male-to-female) fish (barramundi Lates calcarifer) to examine growth in relation to individual variation in the timing of sex change. Growth trajectories of individuals with contrasting life histories were examined to elucidate the direction and extent to which growth rate influences the size and age individuals change sex. Then, the relationships between growth rate, maturation schedules and asymptotic maximum size were explored to identify potential trade-offs between age at female maturity and growth potential. Rapid growth was strongly associated with decreased age at sex change, but this was not accompanied by a decrease in size at sex change. Individuals that were caught as large females grew faster than those caught as males, suggesting that fast-growing individuals ultimately obtain higher fitness and therefore make a disproportionate contribution to population fecundity. These results indicate that individual-level variation in maturation schedules is not reflective of trade-offs between growth and reproduction. Rather, we suggest that conditions experienced during the juvenile phase are likely to be a key determinant of post-maturation fitness. These findings highlight the vulnerability of sex-changing species to future environmental change and harvest.

Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

“…However, here, it was found that DNAm in both sexes became more sex-specific with increasing length, despite the well-established relationship between length and sex in barramundi (i.e., males are small and females are large- Davis, 1982;Guiguen et al, 1994;Moore, 1979;Roberts et al, 2021). DNAm is strongly impacted by a genes' transcriptional state in fish, and other organisms (McGaughey et al, 2014), suggesting that changes in DNAm may arise due to sexspecific transcriptional activity, rather than (or in addition to) DNAm being the cause of changes in transcription of sex-related genes.…”

“…Therefore, based on the regression results and BIC values calculated, length was retained in the subsequent analyses, and age was excluded (Table , Table ). The inclusion of length, but not age, in the model is supported by a recent analysis of barramundi from Western Australia, which identified that sex change is more closely related to length than age (Roberts et al, 2021).…”

“…In addition to truncated DNAm data, these size limits meant that growth curves could not be accurately calculated. Future work measuring changes in DNAm in barramundi below the legal size limit will allow for region‐specific examination of the potential association between growth rate and early sexual maturation, as well as early sex change (Roberts et al, 2021; Warner, 1988).…”

“…Growth and body condition are also highly likely to lead to differences in fecundity and the timing of male‐to‐female sex change in protandrous species, including barramundi (Roberts et al, 2021; Warner, 1988). In barramundi, freshwater flow (e.g., Robins et al, 2006) and food availability (e.g., Russell et al, 2015) have marked effects on growth rate, which is known to lead to differences in the timing of male‐to‐female sex change in this species (Roberts et al, 2021). In the case of temperature, the effect on male‐to‐female sex change may therefore be indirect (e.g., through changes in hormone levels and/or growth rate), direct (e.g., via cellular transduction of temperature cues), or both.…”

“…The underlying drivers of the differences in length-at-sex change in barramundi between regions are unknown, but the phenomenon has been associated with differences in genetic origin and growth rate (Davis, 1984;Roberts et al, 2021), as well as environmental factors, such as temperature and salinity (Athauda & Anderson, 2014;Budd, 2020).…”