Multi-generational fitness legacies of natural immigration: theoretical and empirical perspectives and opportunities.

Abstract

Natural dispersal between populations, and resulting immigration, influences population size and genetic variation and is therefore a key process driving reciprocal interactions between ecological and evolutionary dynamics. Here, population dynamic and evolutionary outcomes fundamentally depend not only on the relative fitnesses of natural immigrants and existing residents, but also on the fitness of their various descendants manifested in natural environments. Yet, the fitnesses of different sets of natural immigrants' descendants have rarely been explicitly or rigorously estimated or rationalised in the context of wild spatially structured populations. We therefore still have surprisingly limited capability to understand or predict the ultimate multi-generational impacts of natural immigration on population and evolutionary dynamics. Key theoretical frameworks that predict fitness outcomes of outcrossing between lineages have been developed and widely utilised in the contexts of agriculture and speciation research. These frameworks have also been applied in conservation genetics research to predict positive (widely termed "heterosis") and negative (widely termed "outbreeding depression") outcomes in the context of genetic rescue of highly inbred populations. However, these frameworks have rarely been utilised explicitly to guide analyses of multi-generational legacies of regular natural immigrants in the context of evolutionary ecology, precluding inferences on the basis of, and implications of, sub-population divergence. Accordingly, to facilitate translation of concepts and inspire new empirical efforts, we first review and synthesise key bodies of theory on multi-generational fitness outcomes, developed in the contexts of crosses between inbred lines and between different species. Such theory reveals how diverse fitness outcomes can be generated by common underlying mechanisms, depending on the genetic architecture of fitness, the forms of genotype-phenotype-fitness maps, and the relative roles of adaptive and non-adaptive mechanisms in population differentiation. Interestingly, such theory predicts particularly diverse fitness outcomes of crosses between weakly diverged lineages, constituting the parameter space where spatially structured populations lie. We then conduct a systematic literature review to assess the degree to which multi-generational outcomes of crosses between structured natural populations have actually been quantified. Our review shows a surprising paucity of empirical studies that quantify multi-generational fitness consequences of outcrossing resulting from natural immigration in the wild. Furthermore, studies undertaking experimental crosses among populations have used inconsistent methodologies, precluding quantitative or even qualitative overall conclusions. To initiate new progress, we outline how long-standing and recent methodological developments, including cutting-edge statistical and genomic tools, could be combined with field data sets to quantify the multi-generational fitness outcomes of crosses between residents and immigrants in nature. We thereby highlight key theoretical and empirical gaps that now need to be filled to further our understanding of dispersal-mediated drivers and constraints on eco-evolutionary dynamics arising in structured populations.