INTRODUCTION
Dispersal of individuals among populations, and resulting immigration, fundamentally underpins key ecological and evolutionary processes that shape populations dynamics and persistence (Lenormand 2002, Lowe et al. 2017). Ecologists have traditionally aimed to understand short and long-term contributions of immigrants to demographic parameters, while evolutionary biologists aim to understand consequences of effective gene flow in mediating adaptive versus non-adaptive evolution and diversification. Yet, the key processes that link these two goals – the underlying causes and resulting magnitudes of fitness of immigrants and their descendants – remain considerably unexplored in both empirical and theoretical studies of metapopulations, and hence in precisely the context where eco-evolutionary implications of dispersal could be most substantial. Here, we synthesize theoretical and empirical knowledge from different disciplines, which provide a framework for advancing understanding of multigenerational fitness effects of immigration in wild metapopulation systems. These advances are fundamental to embedding dispersal, and resulting immigration, as a central driver of reciprocal eco-evolutionary dynamics, thereby facilitating understanding of biodiversity dynamics (Pelletier & Coltman 2018, Pelletier et al. 2009, Reznick et al. 2019, Sutherland et al. 2013).
Immigration can benefit populations by increasing local population size, thereby reducing Allee effects (Stephens & Sutherland 1999) or demographic stochasticity (e.g. Schaub et al. 2013, reviewed in Millon et al. 2019). Whenever immigrants recruit to the adult population and produce viable offspring, further profound short- and long-term impacts on populations can result. Descendants of immigrants can contribute to population growth rates (e.g. Åkesson et al 2016, Ranke et al. 2017) and in turn, larger population sizes can increase the efficiency of natural selection against deleterious alleles (Kimura 1962, Raynes et al. 2018), possibly facilitating evolutionary rescue (Bell 2017, Hoffmann et al. 2021, Stewart et al. 2017). Via introgression of new genetic variants, immigrants can also replenish local genetic variation, alleviating inbreeding and genetic drift load, and increasing individual and population fitness (Adams et al. 2011, Bell 2017, Millon et al. 2019, Stewart et al. 2017, Szucs et al. 2014, Tallmon et al 2004). Yet, conversely, immigrants could reduce population fitness. For instance, introgression of locally maladaptive alleles, and disruptions of genomic coadaptations due to recombination between immigrant and local genomes (Dobzhansky 1950, Soule 1967; see also Kawecki & Ebert 2004), can counter-act local adaptation and generate migration load (Bolnick & Nosil 2007, García-Ramos & Kirkpatrick 1997, Lenormand 2002, Paul et al. 2011, Reid et al. 2021). Net eco-evolutionary impacts of immigration therefore depend on the balance between positive and negative fitness effects of imported genetic variants, and on resulting degrees and rates of introgression, which are contingent on the relative fitnesses of immigrants, residents, and their descendants, and on the frequency in which different descendant categories are naturally produced in populations (Igvarsson & Whitlock 2000, Pfennig & Lachance 2022).
While the frequency and fitness of immigrants is compared to that of existing residents in some demographic studies of natural populations (Millon et al. 2019), explicit estimates for subsequent filial generations (including F1s, F2s and various backcrosses; Fig. 1) are typically lacking. Furthermore, hybrid offspring from immigrant-resident matings are often classified as residents in these comparisons, implying an assumption of equal fitness between residents and the descendants of immigrants. Yet, the fitness of hybrid filial generations will likely differ from that of residents, leading to under- or over-estimation of demographic and genetic contributions of immigrants. Moreover, the relative fitnesses of immigrants, residents and their various descendants (Fig. 1) are ultimately determined by the genetic architecture of fitness and its interactions with environmental conditions, which are shaped by the relative contributions of adaptive and non-adaptive mechanisms to the evolutionary history of population divergence (Barton 2001, Chevin et al. 2014, Dagilis et al. 2019, Lynch 1991, Lynch & Walsh 1998, Rundle & Whitlock 2001, Simon et al. 2018, Schneemann et al. 2020). Therefore, while comprehensive theory is fundamental to predicting the relative fitnesses of subsequent filial generations, empirical studies are essential to test predictions and to elucidate the prevalence and magnitude of effects in natural populations.
Fitness effects of crosses between individuals of different lineages or populations (i.e. outbreeding or outcrossing, terms used interchangeably hereafter) have long been documented and rationalized conceptually in agricultural and [incipient] speciation research (e.g. Crow 1948, Darwin 1876, Dobzhansky 1950, Lynch & Walsh 1998, Orr 1995; Fig. 2). These theoretical developments have also been successfully extended and applied to severely inbred natural populations within the context of ‘genetic rescue’ (Hoffmann et al. 2021, Ingvarsson 2001, Tallmon et al. 2004, Whiteley et al. 2015). However, such theory has rarely been exploited by evolutionary ecologists interested in the consequences of natural dispersal and resulting immigration and gene flow in fragmented populations of single species. Yet, crosses between inbred lines derived from individuals within single or weakly differentiated populations and crosses between isolated species represent two extreme ends of a continuum of genetic divergence where subdivided populations connected by natural dispersal are intermediate (Demuth & Wade 2005, Hughes & Vickery 1974, Simon et al. 2018; Fig. 2). This gap therefore likely simply reflects academic silos, where researchers working on demographic variation and eco-evolutionary dynamics in wild (meta)populations are not focusing explicitly on theory and principles that are central to speciation and agricultural or conservation research.
Hence, to bridge these divides and inspire new activity in evolutionary ecology, we synthesise key aspects of the current empirical and theoretical states of the art in line-cross theory, as primarily developed in the contexts of hybridization or speciation, that aim to rationalize and predict fitness outcomes resulting from complex genetic consequences of multigenerational introgression. We then provide a systematic literature review which highlights that, despite the increasing availability of applicable theory and multigenerational field datasets, fitness outcomes from interbreeding resulting from natural immigration in fragmented populations have still very rarely been explicitly or rigorously estimated. Finally, we highlight conceptual and empirical opportunities and challenges which, in conjunction with newly available methods, can now culminate in comprehensive overview of the consequences of outbreeding spanning the full biological range of divergence.