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.