The relative impact of evolving pleiotropy and mutational correlation on trait divergence

Both pleiotropic connectivity and mutational correlations can restrict the decoupling of traits under divergent selection, but it is unknown which is more important in trait evolution. To address this question, we create a model that permits within-population variation in both pleiotropic connectivity and mutational correlation, and compare their relative importance to trait evolution. Specifically, we developed an individual-based stochastic model where mutations can affect whether a locus affects a trait and the extent of mutational correlations in a population. We find that traits can decouple whether there is evolution in pleiotropic connectivity or mutational correlation, but when both can evolve, then evolution in pleiotropic connectivity is more likely to allow for decoupling to occur. The most common genotype found in this case is characterized by having one locus that maintains connectivity to all traits and another that loses connectivity to the traits under stabilizing selection (subfunctionalization). This genotype is favored because it allows the subfunctionalized locus to accumulate greater effect size alleles, contributing to increasingly divergent trait values in the traits under divergent selection without changing the trait values of the other traits (genetic modularization). These results provide evidence that partial subfunctionalization of pleiotropic loci may be a common mechanism of trait decoupling under regimes of corridor selection.

Coral settlement and recruitment responses to reef fish foraging and trait diversity

The process of coral recruitment is crucial to the healthy functioning of coral reef ecosystems, as well as recovery following disturbances. Fishes are key modulators of this process by feeding on algae and other benthic taxa that compete with corals for benthic space. However, foraging strategies within reef fish assemblages are highly diverse and the effect of foraging diversity on coral recruitment success remains poorly understood. Here, we test how the foraging traits of reef fishes affect coral settlement and juvenile success at Lizard Island, Great Barrier Reef. Using a multi-model inference approach incorporating six metrics of fish assemblage foraging diversity (foraging rates, trait richness, trait evenness, trait divergence, herbivore abundance, and benthic invertivore abundance), we found that herbivore abundance had positive effects on both coral settlement and recruitment success. However, foraging trait diversity had a negative effect on coral settlement but not on recruitment. Coral settlement was higher at sites with less trait diverse fish assemblages, specifically in trait divergence and richness. Moreover, these two trait diversity metrics were stronger predictors of coral settlement success compared to herbivore abundance. Our findings provide evidence that impacts mediated by fish foraging on coral juveniles can potentially be harmful during settlement, but the space-clearing effect overall remains advantageous. We show here that the variation of fish biodiversity across reefs can be a partial driver to spatially uneven patterns of coral recruitment and reef recovery.

Growing up in a new world: trait divergence between rural, urban, and invasive populations of an amphibian urban invader

Cities are focal points of introduction for invasive species. Urban evolution might facilitate the success of invasive species in recipient urban habitats. Here we test this hypothesis by rearing tadpoles of a successful amphibian urban coloniser and invader in a common garden environment. We compared growth rate, morphological traits, swimming performance, and developmental rate of guttural toad tadpoles (Sclerophrys gutturalis) from native rural, native urban, and non-native urban habitats. By measuring these traits across ontogeny, we were also able to compare divergence across different origins as the tadpoles develop. The tadpoles of non-native urban origin showed significantly slower developmental rate (e.g., the proportion of tadpoles reaching Gosner stage 31 or higher was lower at age 40 days) than tadpoles of native urban origin. Yet, tadpoles did not differ in growth rate or any morphological or performance trait examined, and none of these traits showed divergent ontogenetic changes between tadpoles of different origin. These findings suggest that prior adaptation to urban habitats in larval traits likely does not play an important role in facilitating the invasion success of guttural toads into other urban habitats. Instead, we suggest that evolutionary changes in larval traits after colonization (e.g., developmental rate), together with decoupling of other traits and phenotypic plasticity might explain how this species succeeded in colonising extra-limital urban habitats.

Tempo and mode of morphological evolution are decoupled from latitude in birds

The latitudinal diversity gradient is one of the most striking patterns in nature, yet its implications for morphological evolution are poorly understood. In particular, it has been proposed that an increased intensity of species interactions in tropical biota may either promote or constrain trait evolution, but which of these outcomes predominates remains uncertain. Here, we develop tools for fitting phylogenetic models of phenotypic evolution in which the impact of species interactions—namely, competition—can vary across lineages. Deploying these models on a global avian trait dataset to explore differences in trait divergence between tropical and temperate lineages, we find that the effect of latitude on the mode and tempo of morphological evolution is weak and clade- or trait dependent. Our results indicate that species interactions do not disproportionately impact morphological evolution in tropical bird families and question the validity of previously reported patterns of slower trait evolution in the tropics.

Modularity and selection of nectar traits in the evolution of the selfing syndrome in Ipomoea lacunosa (Convolvulaceae)

Although the evolution of the selfing syndrome often involves reductions in floral size, pollen, and nectar, few studies of selfing syndrome divergence have examined nectar. We investigate whether nectar traits have evolved independently of other floral size traits in the selfing syndrome, whether nectar traits diverged due to drift or selection, and the extent to which quantitative trait locus (QTL) analyses predict genetic correlations. We use F5 recombinant inbred lines (RILs) generated from a cross between Ipomoea cordatotriloba and I. lacunosa. We calculate genetic correlations to identify evolutionary modules, test whether traits have been under selection, identify QTLs, and perform correlation analyses to evaluate how well QTL properties reflect the genetic correlations. Nectar and floral size traits form separate genetic clusters. Directional selection has acted to reduce nectar traits in the selfing I. lacunosa. Calculations from QTL properties are consistent with observed genetic correlations. Floral trait divergence during mating system syndrome evolution reflects independent evolution of at least two evolutionary modules: nectar and floral size traits. This independence implies that adaptive change in these modules requires direct selection on both floral size and nectar traits. Our study also supports the expected mechanistic link between QTL properties and genetic correlations.

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.

The genetic architecture and evolution of life-history divergence among perennials in the Mimulus guttatus species complex

Ecological divergence is a fundamental source of phenotypic diversity between closely related species, yet the genetic architecture of most ecologically relevant traits is poorly understood. Differences in elevation can impose substantial divergent selection on both complex, correlated suites of traits (such as life-history), as well as novel adaptations. We use the Mimulus guttatus species complex to assess if the divergence in elevation is accompanied by trait divergence in a group of closely related perennials and determine the genetic architecture of this divergence. We find that divergence in elevation is associated with differences in life-history, as well as a unique trait, the production of rhizomes. The divergence between two perennials is largely explained by few mid-to-large effect quantitative trait loci (QTLs). However, the presence of QTLs with correlated, but opposing effects on multiple traits leads to some hybrids with transgressive trait combinations. Lastly, we find that the genetic architecture of the ability to produce rhizomes changes through development, wherein most hybrids produce rhizomes, but only later in development. Our results suggest that elevational differences may shape life-history divergence between perennials, but aspects of the genetic architecture of divergence may have implications for hybrid fitness in nature.

Asymmetrical reproductive barriers in sympatric jewelflowers: are floral isolation, genetic incompatibilities and floral trait displacement connected?

Floral visitors influence reproductive interactions among sympatric plant species, either by facilitating assortative mating and contributing to reproductive isolation, or by promoting heterospecific pollen transfer, potentially leading to reproductive interference or hybridization. We assessed preference and constancy of floral visitors on two co-occurring jewelflowers [Streptanthus breweri and Streptanthus hesperidis (Brassicaceae)] using field arrays, and quantified two floral rewards potentially important to foraging choice – pollen production and nectar sugar concentration – in a greenhouse common garden. Floral visitors made an abundance of conspecific transitions between S. breweri individuals, which thus experienced minimal opportunities for heterospecific pollen transfer from S. hesperidis. In contrast, behavioural isolation for S. hesperidis was essentially absent due to pollinator inconstancy. This pattern emerged across multiple biotic environments and was unrelated to local density dependence. S. breweri populations that were sympatric with S. hesperidis had higher nectar sugar concentrations than their sympatric congeners, as well as allopatric conspecifics. Previous work shows that S. breweri suffers a greater cost to hybridization than S. hesperidis, and here we find that it also shows asymmetrical floral isolation and floral trait displacement in sympatry. These findings suggest that trait divergence may reduce negative reproductive interactions between sympatric but genetically incompatible relatives.

How does the magnitude of genetic variation affect eco-evolutionary dynamics in character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents population extinction by weakening negative interspecific interactions. When the magnitude of genetic variation is small, however, the speed of trait divergence can be slow and populations may go extinct before the completion of character displacement. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens resource competition and reproductive interference, respectively. We found that the large additive genetic variance is more important for preventing extinction in reproductive character displacement than in ecological character displacement. This is because reproductive interference produces a locally stable coexistence equilibrium with positive frequency-dependence (i.e., minority disadvantage) whereas ecological character displacement results in a globally stable coexistence equilibrium. Furthermore, population extinction becomes less likely when ecological and reproductive character displacement occur simultaneously due to positive covariance between ecological and reproductive traits. Our results suggest that while reproductive character displacement may be rarer than ecological character displacement, it is more likely to occur when there exists positive trait covariance, such as the case of a magic trait in reinforcement of speciation processes.

Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms

Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic, and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%), and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation, and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely canalized physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.