Adaptive and non-adaptive convergent evolution in feather reflectance of California Channel Islands songbirds.

Convergent evolution is widely regarded as a signature of adaptation. However, testing the adaptive consequences of convergent phenotypes is challenging, making it difficult to exclude non-adaptive explanations for convergence. Here, we combined feather reflectance spectra and phenotypic trajectory analyses with visual and thermoregulatory modelling to test the adaptive significance of dark plumage in songbirds of the California Channel Islands. By evolving dark dorsal plumage, island birds are generally less conspicuous to visual-hunting raptors in the island environment than mainland birds. Dark dorsal plumage also reduces the energetic demands associated with maintaining homeothermy in the cool island climate. We also found an unexpected pattern of convergence, wherein the most divergent island populations evolved greater reflectance of near-infrared radiation. However, our heat flux models indicate that elevated near-infrared reflectance is not adaptive. Analysis of feather microstructure suggests that mainland-island differences are related to coloration of feather barbs and barbules rather than their structure. Our results indicate that adaptive and non-adaptive mechanisms interact to drive plumage evolution in this system. This study sheds light on the mechanisms driving the association between dark colour and wet, cold environments across the tree of life, especially in island birds.

Parameterizing mechanistic niche models in biophysical ecology: a review of empirical approaches.

Mechanistic niche models are computational tools developed using biophysical principles to address grand challenges in ecology and evolution, such as the mechanisms that shape the fundamental niche and the adaptive significance of traits. Here, we review the empirical basis of mechanistic niche models in biophysical ecology, which are used to answer a broad array of questions in ecology, evolution and global change biology. We describe the experiments and observations that are frequently used to parameterize these models and how these empirical data are then incorporated into mechanistic niche models to predict performance, growth, survival and reproduction. We focus on the physiological, behavioral and morphological traits that are frequently measured and then integrated into these models. We also review the empirical approaches used to incorporate evolutionary processes, phenotypic plasticity and biotic interactions. We discuss the importance of validation experiments and observations in verifying underlying assumptions and complex processes. Despite the reliance of mechanistic niche models on biophysical theory, empirical data have and will continue to play an essential role in their development and implementation.

Seasonal patterns of dietary partitioning in vertebrates.

Dietary partitioning plays a central role in biological communities, yet the extent of partitioning often varies dramatically over time. Food availability may drive temporal variation in dietary partitioning, but alternative paradigms offer contrasting predictions about its effect. We compiled estimates of dietary overlap between co-occurring vertebrates to test whether partitioning is greater during periods of high or low food abundance. We found that dietary partitioning was generally greatest when food abundance was low, suggesting that competition for limited food drives partitioning. The extent of dietary partitioning in birds and mammals was also related to seasonality in primary productivity. As seasonality increased, partitioning increased during the nonbreeding season for birds and the breeding season for mammals. Although some hypotheses invoke changes in dietary breadth to explain temporal variation in dietary partitioning, we found no association between dietary breadth and partitioning. These results have important implications for the evolution of dietary divergence.

Performance Trade-Offs and Resource Availability Drive Variation in Reproductive Isolation between Sympatrically Diverging Crossbills.

AbstractTheoretical models indicate that speciation, especially when the scope for gene flow is great (e.g., sympatric speciation), is most likely when strong performance trade-offs coincide with reproduction. We tested this classic hypothesis using measures of the strength of three prezygotic reproductive isolating barriers (habitat isolation, reduced immigrant fecundity, and behavioral isolation) between two young (~2,000 years) and sympatric red crossbill (Loxia curvirostra) ecotypes. All three isolating barriers increased with increases in performance trade-offs, with total reproductive isolation varying between 0.72 and 1 (0 represents random mating, and 1 represents complete reproductive isolation). Strong trade-offs led to strong habitat isolation, an inability to breed in the "wrong" habitat, and more assortative flocks, with the latter leading to stronger behavioral isolation. Reproductive isolation decreased as resource availability increased relative to the demands of breeding, with higher resource availabilities eliminating the positive relationship between reproductive isolation and performance trade-offs. This latter result is consistent with previous work suggesting that increasing resource abundance dampens the effect of strong performance trade-offs on evolutionary divergence. Because many organisms, with the notable exception of host-specific phytophagous insects, rely on abundant food resources with weak performance trade-offs while breeding, our results may explain why sympatric speciation is uncommon.

How well do you know your mutation? Complex effects of genetic background on expressivity, complementation, and ordering of allelic effects.

For a given gene, different mutations influence organismal phenotypes to varying degrees. However, the expressivity of these variants not only depends on the DNA lesion associated with the mutation, but also on factors including the genetic background and rearing environment. The degree to which these factors influence related alleles, genes, or pathways similarly, and whether similar developmental mechanisms underlie variation in the expressivity of a single allele across conditions and among alleles is poorly understood. Besides their fundamental biological significance, these questions have important implications for the interpretation of functional genetic analyses, for example, if these factors alter the ordering of allelic series or patterns of complementation. We examined the impact of genetic background and rearing environment for a series of mutations spanning the range of phenotypic effects for both the scalloped and vestigial genes, which influence wing development in Drosophila melanogaster. Genetic background and rearing environment influenced the phenotypic outcome of mutations, including intra-genic interactions, particularly for mutations of moderate expressivity. We examined whether cellular correlates (such as cell proliferation during development) of these phenotypic effects matched the observed phenotypic outcome. While cell proliferation decreased with mutations of increasingly severe effects, surprisingly it did not co-vary strongly with the degree of background dependence. We discuss these findings and propose a phenomenological model to aid in understanding the biology of genes, and how this influences our interpretation of allelic effects in genetic analysis.

Character displacement of a learned behaviour and its implications for ecological speciation.

Cultural evolution may accelerate population divergence and speciation, though most support for this hypothesis is restricted to scenarios of allopatric speciation driven by random cultural drift. By contrast, the role of cultural evolution in non-allopatric speciation (i.e. speciation with gene flow) has received much less attention. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (Loxia curvirostra) complex. Here we focus on Cassia crossbills (Loxia sinesciuris; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a closely related, sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces (maladaptive) heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e. when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over just two decades and by using field experiments to demonstrate that Cassia and red crossbills differentially respond to these evolved differences in call structure, reducing heterospecific flock formation. Moreover, because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5000 years. Our results provide evidence for a largely neglected yet potentially widespread mechanism by which reproductive isolation can evolve between sympatric lineages as a byproduct of adaptive cultural evolution.

Genomes of ubiquitous marine and hypersaline Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments.

Chemolithoautotrophic bacteria from the genera Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira are common, sometimes dominant, isolates from sulfidic habitats including hydrothermal vents, soda and salt lakes and marine sediments. Their genome sequences confirm their membership in a deeply branching clade of the Gammaproteobacteria. Several adaptations to heterogeneous habitats are apparent. Their genomes include large numbers of genes for sensing and responding to their environment (EAL- and GGDEF-domain proteins and methyl-accepting chemotaxis proteins) despite their small sizes (2.1-3.1 Mbp). An array of sulfur-oxidizing complexes are encoded, likely to facilitate these organisms' use of multiple forms of reduced sulfur as electron donors. Hydrogenase genes are present in some taxa, including group 1d and 2b hydrogenases in Hydrogenovibrio marinus and H. thermophilus MA2-6, acquired via horizontal gene transfer. In addition to high-affinity cbb3 cytochrome c oxidase, some also encode cytochrome bd-type quinol oxidase or ba3 -type cytochrome c oxidase, which could facilitate growth under different oxygen tensions, or maintain redox balance. Carboxysome operons are present in most, with genes downstream encoding transporters from four evolutionarily distinct families, which may act with the carboxysomes to form CO2 concentrating mechanisms. These adaptations to habitat variability likely contribute to the cosmopolitan distribution of these organisms.

Assessing the Potential Contributions of Reduced Immigrant Viability and Fecundity to Reproductive Isolation.

Reduced fitness of immigrants from alternative environments is thought to be an important reproductive isolating barrier. Most studies evaluating the importance of the relative fitness of immigrants to speciation have focused on reduced survival of immigrants (i.e., immigrant inviability). However, variation in fecundity appears to have a greater impact on variation in fitness than does variation in viability, suggesting that reduced fecundity of immigrants could act as an important yet largely overlooked reproductive isolating barrier. Using a model and a survey of studies of local adaptation, we evaluate the relative strength of reduced immigrant viability and fecundity as potential causes of reproductive isolation. We found that reduced fecundity as compared to reduced viability as a reproductive isolating barrier should increase in importance as the relative costs of reproduction increase. Consistent with the elevated demands of reproduction reported in the literature, we found that reproductive isolation from reduced immigrant fecundity was of similar magnitude or greater than that from reduced immigrant viability, particularly in the early stages of speciation. These results suggest that the important role of differential fecundity in local adaptation extends to speciation.

Sexual selection's impacts on ecological specialization: an experimental test.

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs-distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.

Strong yet incomplete reproductive isolation in Vermivora is not contradicted by other lines of evidence: A reply to Toews et al.

Toews et al. assert that strong reproductive isolation in Vermivora is inconsistent with other lines of evidence. Here, we discuss how strong yet incomplete reproductive isolation is consistent with other results from this system.

Implications for evolutionary trends from the pairing frequencies among golden-winged and blue-winged warblers and their hybrids.

Extensive range loss for the Golden-winged Warbler (Vermivora chrysoptera) has occurred in areas of intrusion by the Blue-winged Warbler (V. cyanoptera) potentially related to their close genetic relationship. We compiled data on social pairing from nine studies for 2,679 resident Vermivora to assess evolutionary divergence. Hybridization between pure phenotypes occurred with 1.2% of resident males for sympatric populations. Pairing success rates for Golden-winged Warblers was 83% and for Blue-winged Warblers was 77%. Pairing success for the hybrid Brewster's Warbler was significantly lower from both species at 54%, showing sexual selection against hybrids. Backcross frequencies for Golden-winged Warblers at 4.9% were significantly higher than for Blue-winged Warblers at 1.7%. More frequent backcrossing by Golden-winged Warblers, which produces hybrid phenotypes, may contribute to the replacement of Golden-winged by Blue-winged Warblers. Reproductive isolation due to behavioral isolation plus sexual selection against hybrids was 0.960. Our analyses suggest that plumage differences are the main driving force for this strong isolation with reduced hybrid fitness contributing to a lesser degree. The major impact of plumage differences to reproductive isolation is compatible with genomic analyses (Current Biology, 2016, 26, 2313), which showed the largest genetic difference between these phenotypes occurred with plumage genes. These phenotypes have maintained morphological, behavioral, and ecological differences during two centuries of hybridization. Our estimate of reproductive isolation supports recognition of these phenotypes as two species. The decline and extirpation of the Golden-winged Warbler in almost all areas of recent sympatry suggest that continued coexistence of both species will require eco-geographic isolation.

The behavioral repertoire of Drosophila melanogaster in the presence of two predator species that differ in hunting mode.

The fruit fly, Drosophila melanogaster, has proven to be an excellent model organism for genetic, genomic and neurobiological studies. However, relatively little is known about the natural history of D. melanogaster. In particular, neither the natural predators faced by wild populations of D. melanogaster, nor the anti-predatory behaviors they may employ to escape and avoid their enemies have been documented. Here we observe and describe the influence of two predators that differ in their mode of hunting: zebra jumping spiders, Salticus scenicus (active hunters) and Chinese praying mantids, Tenodera sinensis (ambush predators) on the behavioral repertoire of Drosophila melanogaster. We documented three particularly interesting behaviors: abdominal lifting, stopping, and retreat-which were performed at higher frequency by D. melanogaster in the presence of predators. While mantids had only a modest influence on the locomotory activity of D. melanogaster, we observed a significant increase in the overall activity of D. melanogaster in the presence of jumping spiders. Finally, we observed considerable among-individual behavioral variation in response to both predators.

An Alternative to Adaptation by Sexual Selection: Habitat Choice.

Adaptation in mating signals and preferences has generally been explained by sexual selection. We propose that adaptation in such mating traits might also arise via a non-mutually exclusive process wherein individuals preferentially disperse to habitats where they experience high mating performance. Here we explore the evolutionary implications of this process.

Comment on Van Belleghem et al. 2016: Habitat choice mechanisms in speciation and other forms of diversification.

Several mechanisms of habitat choice can contribute to speciation. Empirical studies of habitat choice mechanisms provide important insights into the relative roles of these mechanisms in speciation. A recent paper by Van Belleghem and colleagues characterizes the mechanistic basis of a component of habitat choice-departure behavior-in two salt marsh beetle ecotypes that inhabit different environments. The authors compare the departure behavior between the two ecotypes in response to an environmental cue and find that ecotypes differ in their tendency to depart in response to this cue and that the environment experienced by immature beetles affects the departure behavior of adult beetles. The authors conclude that such plastic behavioral differences between ecotypes should reduce gene flow and thereby facilitate reproductive isolation between ecotypes. We question whether such a mechanism of departure behavior would effectively reduce gene flow between ecotypes. Furthermore, their study highlights the need for some clarification of habitat choice mechanisms and related concepts, as conceptual inconsistencies are common in the literature. Here, we clarify major mechanisms of habitat choice and discuss how each mechanism might facilitate speciation. We emphasize that future empirical work should be guided by careful consideration of the natural history of species under study.