Gene flow improves fitness at a range edge under climate change
Populations at the margins of a species geographic range are often thought to be poorly adapted to their environment. According to theoretical predictions, gene flow can inhibit these range edge populations if it disrupts adaptation to local conditions. Alternatively, if range edge populations are small or isolated, gene flow can provide beneficial genetic variation, and may facilitate adaptation to environmental change. We tested these competing predictions in the annual wildflower Clarkia pulchella using greenhouse crosses to simulate gene flow from sources across the geographic range into two populations at the northern range margin. We planted these between-population hybrids in common gardens at the range edge, and evaluated how genetic differentiation and climatic differences between edge populations and gene flow sources affected lifetime fitness. During an anomalously warm study year, gene flow from populations occupying historically warm sites improved fitness at the range edge, and plants with one or both parents from warm populations performed best. The effects of the temperature provenance of gene flow sources were most apparent at early life history stages, but precipitation provenance also affected reproduction. We also found benefits of gene flow that were independent of climate: after climate was controlled for, plants with parents from different populations performed better at later lifestages than those with parents from the same population, indicating that gene flow may improve fitness via relieving homozygosity. Further supporting this result, we found that increasing genetic differentiation of parental populations had positive effects on fitness of hybrid seeds. Gene flow from warmer populations, when it occurs, is likely to contribute adaptive genetic variation to populations at the northern range edge as the climate warms. On heterogeneous landscapes, climate of origin may be a better predictor of gene flow effects than geographic proximity.\n\nImpact summaryWhat limits species geographic ranges on the landscape? One process of interest when trying to answer this question is gene flow, which is the movement of genetic material between populations, as might occur in plants when seeds or pollen move across the landscape. One hypothesis that has been proposed is that gene flow from populations in other environments prevents populations at range edges from adapting to their local habitats. Alternatively, it has been suggested that these populations might benefit from gene flow, as it would provide more genetic material for natural selection to act upon.\n\nWe tested these predictions in an annual wildflower, Clarkia pulchella. We simulated gene flow by pollinating plants from the range edge with pollen from other populations. Then we planted the resulting seeds into common gardens in the home sites of the range edge populations and recorded their germination, survival, and reproduction. The weather during our experiment was much warmer than historic averages in our garden sites, and perhaps because of this, we found that gene flow from warm locations improved the performance of range edge populations. This result highlights the potential role of gene flow and dispersal in aiding adaptation to warming climates. We also found some positive effects of gene flow that were independent of climate. Even after we statistically controlled for adaptation to temperature and precipitation, plants that were the result of gene flow pollinations produced more seeds and fruits than plants with both parents from the same population. Rather than preventing adaptation, in our experiment, gene flow generally had positive effects on fitness.