Natural developmental temperatures of ectotherms: A systematic map and comparative analysis

Rebecca Raynal , Patrice Pottier , Shinichi Nakagawa, Lisa Schwanz

In ectothermic animals, physiological processes are highly sensitive to environmental temperatures. Developmental temperatures, in particular, have large and long-lasting impacts on ectotherm phenotypes. However, most phenotypic responses are studied in the laboratory, and may not accurately reflect ecological impacts in natural environments. In this study, we provide the first synthesis of natural oviposition site temperatures in wild ectothermic populations by collating and analysing 64 years (1958-2022) of published data. First, we conducted a systematic review to explore the history and trends in the field. Second, we examined how the mean and among-site variation in temperatures varied across latitude, habitats (land/water), and taxonomic groups (arthropods, fish, amphibians, and reptiles). Third, we performed a meta-analysis to investigate the extent to which temperatures of natural oviposition sites influence the phenotypes of newly hatched ectotherms. We found a large taxonomic bias towards reptile model species, with few studies from fishes, amphibians, and arthropods. This bias towards reptile species can be explained by a historical focus on targeted research questions (e.g. temperature-dependent sex determination) and a lag in technological developments required to measure nest temperatures in other taxa (e.g. waterproof miniature dataloggers). We found no evidence for a correlation between mean oviposition site temperatures and latitude, but the temperature variability among oviposition sites within a population increases significantly with latitude. We also found that ectotherms laying eggs in water have a steeper decline in oviposition site temperatures with latitude than those that lay their eggs on land. These findings suggest that mothers select oviposition site temperatures that likely optimise embryonic development regardless of local climate, yet maternal selection behaviour may be less effective for those laying eggs in the water and at higher latitudes. Strikingly, studies quantifying the impacts of natural oviposition site temperatures on hatchling development or hatching success are rare (N = 46 studies) and biased towards a few (N = 19) reptile or arthropod species. However, our meta-analysis revealed small-to-large negative correlations between oviposition site temperatures and incubation duration and hatching success (Zr = -0.580 and -0.076, respectively). This suggests that the widely reported impacts of developmental temperatures on hatchling phenotype described in laboratory studies will translate to impacts in the wild. However, existing taxonomic biases challenge the generalisability of these findings across ectotherms. We provide recommendations and highlight novel technological advances that will help fill knowledge gaps and complement our understanding of the impacts of temperature on wild ectotherms.