Expansion load reduces fitness at the range margin of an invasive plant

Abstract

Genetic drift and natural selection jointly shape how populations evolve during range expansion, yet their joint influence on fitness at expanding range margins is rarely examined. Serial founder events during range expansion may amplify genetic drift and result in the accumulation (or greater expression) of deleterious mutations at range margins, termed expansion load. Conversely, natural selection should lead to local adaptation during expansion provided that populations harbor adequate genetic variation. We used a manipulative transplant experiment, genome-wide SNP data, and demographic surveys of the invasive plant, commontansy (Tanacetum vulgare), to evaluate evidence for expansion load and local adaptation during ca. 150 years of invasion in Minnesota, U.S.A. The common garden occurred near the southern range margin and included 16 populations that span (1) a chronosequence of invasion from northeastern MN (invasion core) to southern and western range margins and (2) environmental gradients in temperature and precipitation. We also manipulated temperature and precipitation to test whether environmental stress amplified the expression of expansion load or revealed population differentiation in climate adaptation. Population fitness declined strongly with distance from the invasion core, consistent with the accumulation of expansion load. This finding was corroborated by analyses of 173 populations that showed an increase in homozygosity (F) and a decrease in population size from the invasion core to range margins. We did not find any evidence of local adaptation; a strong positive relationship between population mean fitness and environmental distance was indicative of maladaptation. While the elevated temperature manipulation reduced fitness, it did not amplify the expression of expansion load. Taken together, our results are consistent with the hypothesis that serial population bottlenecks and strong genetic drift led to expansion load and reduced fitness at range margins. Teaser TextSpecies geographic ranges are dynamic over geologic time scales but may also shift rapidly in response to climate change and for invasive species. While range shifts are often viewed only through an ecological lens, the extent and pace of range expansion may be significantly modulated by evolutionary processes. We disentangled the influence of genetic drift and natural selection on population fitness across an invasion chronosequence (spanning ca. 150 years) for the herbaceous plant common tansy (Tanacetum vulgare). Our synthesis of analyses of a field transplant experiment, genome-wide SNP data, and demographic surveys provided evidence consistent with the accumulation of expansion load at leading range edges. While theory often predicts that local adaptation should occur readily in response to novel environments, our results were consistent with local maladaptation. Our findings emphasize the importance of stochastic processes in shaping the geographic distribution of species and their capacity to shift with changing environments.