Rapid ecological and evolutionary divergence during a poleward range expansion

Abstract

Understanding how species distributions respond to environmental change is a key question in ecology and evolution. While many species are shifting their ranges, the mechanisms driving the extent and rate of these shifts, and the consequences of their establishment in a novel environment, are often poorly understood. Particularly interesting groups of organisms to study in this context are those that have shifted their distributions faster than warming average temperatures alone can explain. Our study investigates whether adaptation to colder temperatures in novel northern environments—and associated life history trade-offs across different life stages—explains this apparent mismatch between climate change and the pace of range expansion. Unlike many range-expanding taxa, our focal species, the wasp spider Argiope bruennichi, disperses passively via ballooning, and as a generalist mesopredator, its expansion is not limited by host plant availability and can exert significant bottom-up and top-down ecosystem effects, making it of particular interest. We integrated analyses of adult phenology, morphology, offspring cold tolerance, and genome-wide variation to test which traits are likely driven by adaptation to colder conditions or whether phenotypic plasticity drives the rapid northward expansion. Females matured earlier at smaller sizes at the range edge. The lack of a concurrent reduction in fecundity suggests that genetic adaptation plays a role. Hatched juveniles that overwintered in their egg sacs were subjected to a reciprocal common garden experiment that simulated either core or edge winter temperatures. Edge-origin spiderlings exhibited lower overall overwinter survival, but the surviving ones had lower lethal temperatures and enhanced supercooling ability than their core-origin counterparts. Furthermore, metabolomic profiles revealed that cold stress-induced accumulation of amino acids and myo-inositol likely contributes to improved cold tolerance. A genome-wide analysis delineated two distinct genetic clusters across Europe, separated by central Germany, and showed that genetic variation is linked to winter climate and seasonality gradients. Overall, our data support genetic differentiation as a major driver of the observed differences, coupled with considerable phenotypic plasticity. Our integrated approach underscores the necessity of assessing trait evolution across life stages to understand how organisms overcome climatic barriers, thus elucidating the mechanisms underlying rapid range expansion.