Mitochondrial-nuclear variation for metabolic plasticity with potential consequences for invasion success in New Zealand mud snails

Abstract

Metabolic rate is an emergent organismal trait that integrates energetic costs of living and influences species distributions and response to climate change. For ectotherms, metabolic rate is likely shaped by interactions between mitochondrial and nuclear genomes and environmental temperature. Variation in reproductive mode (e.g., asexual vs. sexual reproduction) can enhance or interfere with cross-generational transmission of these interactions, with implications for evolutionary responses to selection on standing genetic variation for metabolism-related traits. We leveraged known patterns of mitochondrial-nuclear discordance in a global invader, the snail Potamopyrgus antipodarum, to measure thermal plasticity of metabolic rate in invasive vs. native asexual lineages that combined multiple mitochondrial haplotypes with nuclear genomic variation from distinct lake populations. Native lineages harbored significant mitochondrial-nuclear variation for metabolic plasticity, with some genotypes maintaining low metabolic rates at high temperature. Invasive lineages contained only a small subset of this variation, with non-plastic and lower metabolic rates relative to native lineages at high temperature. Together, these data indicate that mitochondrial-nuclear-environment interactions contribute to variation in the metabolic rate of asexual lineages. Our results also demonstrate that invasive lineages have metabolic phenotypes that could facilitate successful colonization of aquatic habitats via decreased maintenance metabolism under high temperatures.