Temperature and sex shape reproductive barriers in a climate change hotspot

Abstract

Climate change is shifting species ranges and altering reproductive interactions within those ranges, offering closely-related species new scope to mate and potentially hybridize. Predicting hybridization and its outcomes requires assessing the interplay of biological and climatic factors that mediate reproductive barriers across life stages. However, few studies have done so across the range of environments that parents and offspring potentially encounter in nature, as is crucial to understand the environmental sensitivity of reproductive isolation and its fate under climate change. We set out to assess prezygotic and postzygotic reproductive barriers, and their dependence on temperature and sex, in sister species of a marine tubeworm (Galeolaria) from a sentinel region for climate change impacts in southern Australia. We performed reciprocal crosses within- and between-species using replicate populations, and assessed fertility of crosses, survival of embryos, and survival of larvae, at five temperatures spanning the thermal ranges of populations in nature. We found that barriers were weak and independent of temperature at fertilization, but stronger and more temperature-sensitive at larval development, as species diverged in thermal tolerance. Barriers were asymmetric between reciprocal hybrids, moreover, suggesting a complex interplay between thermal adaptation in parental lineages and maternal inheritance of factors (e.g., mitochondria, endosymbionts) that influence hybrid viability across temperatures. Together, our findings provide new insights into the roles of temperature and sex in reproductive barriers across early life stages, and point to shifting strengths of reproductive isolation in future climates.