Ecology and the Origin of Nonephemeral Species.

AbstractResearch over the past three decades has shown that ecology-based extrinsic reproductive barriers can rapidly arise to generate incipient species-but such barriers can also rapidly dissolve when environments change, resulting in incipient species collapse. Understanding the evolution of unconditional, "intrinsic" reproductive barriers is therefore important for understanding the longer-term buildup of biodiversity. In this article, we consider ecology's role in the evolution of intrinsic reproductive isolation. We suggest that this topic has fallen into a gap between disciplines: while evolutionary ecologists have traditionally focused on the rapid evolution of extrinsic isolation between co-occurring ecotypes, speciation geneticists studying intrinsic isolation in other taxa have devoted little attention to the ecological context in which it evolves. We argue that for evolutionary ecology to close this gap, the field will have to expand its focus beyond rapid adaptation and its traditional model systems. Synthesizing data from several subfields, we present circumstantial evidence for and against different forms of ecological adaptation as promoters of intrinsic isolation and discuss alternative forces that may be significant. We conclude by outlining complementary approaches that can better address the role of ecology in the evolution of nonephemeral reproductive barriers and, by extension, less ephemeral species.

Digest: The non-redundancy of non-ephemeral reproductive isolation.

What factors determine the stability of intrinsic reproductive barriers in the face of hybridization? In a set of theoretical analyses, Xiong and Mallet (2022) show that intrinsic incompatibilities are more prone to collapse when the incompatible genotypes encode biological functions with redundant genetic bases. These findings suggest that stable reproductive barriers often will be based on non-redundant genetic complexes that evolve among diverging lineages.

The role of divergent ecological adaptation during allopatric speciation in vertebrates.

After decades of debate, biologists today largely agree that most speciation events require an allopatric phase (that is, geographic separation), but the role of adaptive ecological divergence during this critical period is still unknown. Here, we show that relatively few allopatric pairs of birds, mammals, or amphibians exhibit trait differences consistent with models of divergent adaptation in each of many ecologically relevant traits. By fitting new evolutionary models to numerous sets of sister-pair trait differences, we find that speciating and recently speciated allopatric taxa seem to overwhelmingly evolve under similar rather than divergent macro-selective pressures. This contradicts the classical view of divergent adaptation as a prominent driver of the early stages of speciation and helps synthesize two historical controversies regarding the ecology and geography of species formation.

Geographic contact drives increased reproductive isolation in two cryptic Empidonax flycatchers.

Geographic contact between sister lineages often occurs near the final stages of speciation, but its role in speciation's completion remains debated. Reproductive isolation may be essentially complete prior to secondary contact. Alternatively, costly interactions between partially reproductively isolated species - such as maladaptive hybridization or competition for resources - may select for divergence, increasing reproductive isolation and driving speciation toward completion. Here, we use coalescent demographic modelling and whole-genome data sets to show that a period of contact and elevated hybridization between sympatric eastern North American populations of two cryptic bird species preceded a major increase in reproductive isolation between these populations within the last 10,000 years. In contrast, substantial introgression continues to the present in a western contact zone where geographic overlap is much narrower and probably of more recent origin. In the sympatric eastern region where reproductive isolation has increased, it is not accompanied by character displacement in key morphometric traits, plumage coloration, or ecological traits. While the precise trait and underlying mechanism driving increased reproductive isolation remains unknown, we discuss several possibilities and outline avenues for future research. Overall, our results highlight how demographic models can reveal the geographic context in which reproductive isolation was completed, and demonstrate how contact can accelerate the final stages of speciation.

Character displacement drives trait divergence in a continental fauna.

Coexisting (sympatric) pairs of closely related species are often characterized by exaggerated trait differences. This widespread pattern is consistent with adaptation for reduced similarity due to costly interactions (i.e., "character displacement")-a classic hypothesis in evolutionary theory. But it is equally consistent with a community assembly bias in which lineages with greater trait differences are more likely to establish overlapping ranges in the first place (i.e., "species sorting"), as well as with null expectations of trait divergence through time. Few comparative analyses have explicitly modeled these alternatives, and it remains unclear whether trait divergence is a general prerequisite for sympatry or a consequence of interactions between sympatric species. Here, we develop statistical models that allow us to distinguish the signature of these processes based on patterns of trait divergence in closely related lineage pairs. We compare support for each model using a dataset of bill shape differences in 207 pairs of New World terrestrial birds representing 30 avian families. We find that character displacement models are overwhelmingly supported over species sorting and null expectations, indicating that exaggerated bill shape differences in sympatric pairs result from enhanced divergent selection in sympatry. We additionally detect a latitudinal gradient in character displacement, which appears strongest in the tropics. Our analysis implicates costly species interactions as powerful drivers of trait divergence in a major vertebrate fauna. These results help substantiate a long-standing but equivocally supported linchpin of evolutionary theory.

A Comparative Test for Divergent Adaptation: Inferring Speciation Drivers from Functional Trait Divergence.

AbstractEcological differentiation between lineages is widely considered to be an important driver of speciation, but support for this hypothesis is mainly derived from the detailed study of a select set of model species pairs. Mounting evidence from nonmodel taxa, meanwhile, suggests that speciation often occurs with minimal differentiation in ecology or ecomorphology, calling into question the true contribution of divergent adaptation to species richness in nature. To better understand divergent ecological adaptation and its role in speciation generally, researchers require a comparative approach that can distinguish its signature from alternative processes, such as drift and parallel selection, in data sets containing many species pairs. Here we introduce new statistical models of divergent adaptation in the continuous traits of paired lineages. In these models, ecomorphological characters diverge as two lineages adapt toward alternative phenotypic optima following their departure from a common ancestor. The absolute distance between optima measures the extent of divergent selection and provides a basis for interpretation. We encode the models in the new R package diverge and extend them to allow the distance between optima to vary across continuous and categorical variables. We test model performance using simulation and demonstrate model application using published data sets of trait divergence in birds and mammals. Our framework provides the first explicit test for signatures of divergent selection in trait divergence data sets, and it will enable empiricists from a wide range of fields to better understand the dynamics of divergent adaptation and its prevalence in nature beyond just our best-studied model systems.