Perspective: Reproductive Isolation Caused by Natural Selection Against Immigrants From Divergent Habitats

Abstract

The classification of reproductive isolating barriers laid out by Dobzhansky and Mayr has motivated and structured decades of research on speciation. We argue, however, that this classification is incomplete and that the unique contributions of a major source of reproductive isolation have often been overlooked. Here, we describe reproductive barriers that derive from the reduced survival of immigrants upon reaching foreign habitats that are ecologically divergent from their native habitat. This selection against immigrants reduces encounters and thus mating opportunities between individuals from divergently adapted populations. It also reduces the likelihood that successfully mated immigrant females will survive long enough to produce their hybrid offspring. Thus, natural selection against immigrants results in distinctive elements of premating and postmating reproductive isolation that we hereby dub "immigrant inviability." We quantify the contributions of immigrant inviability to total reproductive isolation by examining study systems where multiple components of reproductive isolation have been measured and demonstrate that these contributions are frequently greater than those of traditionally recognized reproductive barriers. The relevance of immigrant inviability is further illustrated by a consideration of population-genetic theory, a review of selection against immigrant alleles in hybrid zone studies, and an examination of its participation in feedback loops that influence the evolution of additional reproductive barriers. Because some degree of immigrant inviability will commonly exist between populations that exhibit adaptive ecological divergence, we emphasize that these barriers play critical roles in ecological modes of speciation. We hope that the formal recognition of immigrant inviability and our demonstration of its evolutionary importance will stimulate more explicit empirical studies of its contributions to speciation.

Long‐term acclimation to reciprocal light conditions suggests depth‐related selection in the marine foundation species Posidonia oceanica

“…In addition, despite the potential free dispersion of clonal fragments within the meadow, the strong separation between shallow and deep stands indicates that recruitment of adult individuals coming from other depths is rare. Multiple isolating mechanisms (Nosil et al., 2005) may operate along the depth gradient by not only promoting the reproductive isolation but also affecting the survival of immigrants. Although in our experiment clones collected at different depths showed phenotypic buffering and partial acclimation to the reciprocal light conditions in the experimental time frame, we must consider that light is only one of the environmental factors changing between different depths.…”

Of “Host Forms” and Host Races: Terminological Issues in Ecological Speciation

“…That fact notwithstanding, I have used it in prior publications when referring to the populations of N. bebbianae leaf beetles associated with their six different host plants [11,29,31,[35][36][37][38][39][40][41][42]. As my prior use of "host form" in papers and talks has not led to its broader adoption by the field, I hope that this paper will more effectively encourage such usage (!).…”

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

“…Despite such evidence of local adaptation from common‐garden studies, patterns of population structure observed at nuclear loci are often considered to result from neutral processes affecting the whole genome, including genetic drift, gene flow, and past demographic events (e.g., recent range contractions and expansions). A more recent view is that natural selection can also affect genomewide population divergence if gene flow among ecologically divergent habitats is reduced because of selection acting against nonlocally adapted migrants (Hendry, 2004; Nosil, Vines, & Funk, 2005), or because of other nonadaptive processes (Wang & Bradburd, 2014). These processes can result in “isolation‐by‐environment” (IBE) patterns, that is, an increase in among‐population genetic differentiation with increasing environmental distance, independent of geographic distance (Wang & Bradburd, 2014; Wang & Summers, 2010).…”