Speciation-by-Extinction.

Extinction is a dominant force shaping patterns of biodiversity through time; however its role as a catalyst of speciation through its interaction with intraspecific variation has been overlooked. Here, we synthesize ideas alluded to by Darwin and others into the model of "speciation-by-extinction" in which speciation results from the extinction of intermediate populations within a single geographically variable species. We explore the properties and distinguishing features of speciation-by-extinction with respect to other established speciation models. We demonstrate its plausibility by showing that the experimental extinction of populations within variable species can result in speciation. The prerequisites for speciation-by-extinction, geographically structured intraspecific variation and local extinction, are ubiquitous in nature. We propose that speciation-by-extinction may be a prevalent, but underappreciated, speciation mechanism.

Rethinking Gloger's Rule: Climate, Light Environments, and Color in a Large Family of Tropical Birds (Furnariidae).

AbstractEcogeographic rules provide a framework within which to test evolutionary hypotheses of adaptation. Gloger's rule predicts that endothermic animals should have darker colors in warm/rainy climates. This rule also predicts that animals should be more rufous in warm/dry climates, the so-called complex Gloger's rule. Empirical studies frequently demonstrate that animals are darker in cool/wet climates rather than in warm/wet climates. Furthermore, sensory ecology predicts that, to enhance crypsis, animals should be darker in darker light environments. We aimed to disentangle the effects of climate and light environments on plumage color in the large Neotropical passerine family Furnariidae. We found that birds in cooler and rainier climates had darker plumage even after controlling for habitat type. Birds in darker habitats had darker plumage even after controlling for climate. The effects of temperature and precipitation interact so that the negative effect of precipitation on brightness is strongest in cool temperatures. Finally, birds tended to be more rufous in warm/dry habitats but also, surprisingly, in cool/wet locales. We suggest that Gloger's rule results from complementary selective pressures arising from myriad ecological factors, including crypsis, thermoregulation, parasite deterrence, and resistance to feather abrasion.

The evolution of a tropical biodiversity hotspot.

The tropics are the source of most biodiversity yet inadequate sampling obscures answers to fundamental questions about how this diversity evolves. We leveraged samples assembled over decades of fieldwork to study diversification of the largest tropical bird radiation, the suboscine passerines. Our phylogeny, estimated using data from 2389 genomic regions in 1940 individuals of 1283 species, reveals that peak suboscine species diversity in the Neotropics is not associated with high recent speciation rates but rather with the gradual accumulation of species over time. Paradoxically, the highest speciation rates are in lineages from regions with low species diversity, which are generally cold, dry, unstable environments. Our results reveal a model in which species are forming faster in environmental extremes but have accumulated in moderate environments to form tropical biodiversity hotspots.

Evolution of breeding plumages in birds: A multiple-step pathway to seasonal dichromatism in New World warblers (Aves: Parulidae).

Many species of birds show distinctive seasonal breeding and nonbreeding plumages. A number of hypotheses have been proposed for the evolution of this seasonal dichromatism, specifically related to the idea that birds may experience variable levels of sexual selection relative to natural selection throughout the year. However, these hypotheses have not addressed the selective forces that have shaped molt, the underlying mechanism of plumage change. Here, we examined relationships between life-history variation, the evolution of a seasonal molt, and seasonal plumage dichromatism in the New World warblers (Aves: Parulidae), a family with a remarkable diversity of plumage, molt, and life-history strategies. We used phylogenetic comparative methods and path analysis to understand how and why distinctive breeding and nonbreeding plumages evolve in this family. We found that color change alone poorly explains the evolution of patterns of biannual molt evolution in warblers. Instead, molt evolution is better explained by a combination of other life-history factors, especially migration distance and foraging stratum. We found that the evolution of biannual molt and seasonal dichromatism is decoupled, with a biannual molt appearing earlier on the tree, more dispersed across taxa and body regions, and correlating with separate life-history factors than seasonal dichromatism. This result helps explain the apparent paradox of birds that molt biannually but show breeding plumages that are identical to the nonbreeding plumage. We find support for a two-step process for the evolution of distinctive breeding and nonbreeding plumages: That prealternate molt evolves primarily under selection for feather renewal, with seasonal color change sometimes following later. These results reveal how life-history strategies and a birds' environment act upon multiple and separate feather functions to drive the evolution of feather replacement patterns and bird coloration.

Macroevolutionary bursts and constraints generate a rainbow in a clade of tropical birds.

BACKGROUND: Bird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint. RESULTS: We found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst. CONCLUSIONS: Overall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.

Isolation by distance, not incipient ecological speciation, explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis, Line-cheeked Spinetail) despite near threefold body size change across an environmental gradient.

During the process of ecological speciation, reproductive isolation results from divergent natural selection and leads to a positive correlation between genetic divergence and adaptive phenotypic divergence, that is, isolation by adaptation (IBA). In natural populations, phenotypic differentiation is often autocorrelated with geographic distance, making IBA difficult to distinguish from the neutral expectation of isolation by distance (IBD). We examined these two alternatives in a dramatic case of clinal phenotypic variation in an Andean songbird, the Line-cheeked Spinetail (Cranioleuca antisiensis). At its geographic extremes, this species shows a near threefold difference in body mass (11.5 to 31.0 g) with marked plumage differences. We analysed phenotypic, environmental and genetic data (5,154 SNPs) from 172 individuals and 19 populations sampled along its linear distribution in the Andes. We found that body mass was tightly correlated with environmental temperature, consistent with local adaptation as per Bergmann's rule. Using a PST -FST analysis, we found additional support for natural selection driving body mass differentiation, but these results could also be explained by environment-mediated phenotypic plasticity. When we assessed the relative support for patterns of IBA and IBD using variance partitioning, we found that IBD was the best explanation for genetic differentiation along the cline. Adaptive phenotypic or environmental divergence can reduce gene flow, a pattern interpreted as evidence of ecological speciation's role in diversification. Our results provide a counterexample to this interpretation. Despite conditions conducive to ecological speciation, our results suggest that dramatic size and environmental differentiation within C. antisiensis are not limiting gene flow.

Correction: A latitudinal phylogeographic diversity gradient in birds.

[This corrects the article DOI: 10.1371/journal.pbio.2001073.].

Positive association between population genetic differentiation and speciation rates in New World birds.

An implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, but its significance as a rate-limiting control on phylogenetic speciation dynamics remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. By pairing population genetics datasets from 173 New World bird species (>17,000 individuals) with phylogenetic estimates of speciation rate, we show that the population differentiation rates within species are positively correlated with their speciation rates over long timescales. Although population differentiation rate explains relatively little of the variation in speciation rate among lineages, the positive relationship between differentiation rate and speciation rate is robust to species-delimitation schemes and to alternative measures of both rates. Population differentiation occurs at least three times faster than speciation, which suggests that most populations are ephemeral. Speciation and population differentiation rates are more tightly linked in tropical species than in temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest that the processes responsible for population differentiation are tied to those that underlie broad-scale patterns of diversity.

A latitudinal phylogeographic diversity gradient in birds.

High tropical species diversity is often attributed to evolutionary dynamics over long timescales. It is possible, however, that latitudinal variation in diversification begins when divergence occurs within species. Phylogeographic data capture this initial stage of diversification in which populations become geographically isolated and begin to differentiate genetically. There is limited understanding of the broader implications of intraspecific diversification because comparative analyses have focused on species inhabiting and evolving in restricted regions and environments. Here, we scale comparative phylogeography up to the hemisphere level and examine whether the processes driving latitudinal differences in species diversity are also evident within species. We collected genetic data for 210 New World bird species distributed across a broad latitudinal gradient and estimated a suite of metrics characterizing phylogeographic history. We found that lower latitude species had, on average, greater phylogeographic diversity than higher latitude species and that intraspecific diversity showed evidence of greater persistence in the tropics. Factors associated with species ecologies, life histories, and habitats explained little of the variation in phylogeographic structure across the latitudinal gradient. Our results suggest that the latitudinal gradient in species richness originates, at least partly, from population-level processes within species and are consistent with hypotheses implicating age and environmental stability in the formation of diversity gradients. Comparative phylogeographic analyses scaled up to large geographic regions and hundreds of species can show connections between population-level processes and broad-scale species-richness patterns.

Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae).

Rapid diversification may be caused by ecological adaptive radiation via niche divergence. In this model, speciation is coupled with niche divergence and lineage diversification is predicted to be correlated with rates of niche evolution. Studies of the role of niche evolution in diversification have generally focused on ecomorphological diversification but climatic-niche evolution may also be important. We tested these alternatives using a phylogeny of 298 species of ovenbirds (Aves: Furnariidae). We found that within Furnariidae, variation in species richness and diversification rates of subclades were best predicted by rate of climatic-niche evolution than ecomorphological evolution. Although both are clearly important, univariate regression and multivariate model averaging more consistently supported the climatic-niche as the best predictor of lineage diversification. Our study adds to the growing body of evidence, suggesting that climatic-niche divergence may be an important driver of rapid diversification in addition to ecomorphological evolution. However, this pattern may depend on the phylogenetic scale at which rate heterogeneity is examined.

Similarity thresholds used in DNA sequence assembly from short reads can reduce the comparability of population histories across species.

Comparing inferences among datasets generated using short read sequencing may provide insight into the concerted impacts of divergence, gene flow and selection across organisms, but comparisons are complicated by biases introduced during dataset assembly. Sequence similarity thresholds allow the de novo assembly of short reads into clusters of alleles representing different loci, but the resulting datasets are sensitive to both the similarity threshold used and to the variation naturally present in the organism under study. Thresholds that require high sequence similarity among reads for assembly (stringent thresholds) as well as highly variable species may result in datasets in which divergent alleles are lost or divided into separate loci ('over-splitting'), whereas liberal thresholds increase the risk of paralogous loci being combined into a single locus ('under-splitting'). Comparisons among datasets or species are therefore potentially biased if different similarity thresholds are applied or if the species differ in levels of within-lineage genetic variation. We examine the impact of a range of similarity thresholds on assembly of empirical short read datasets from populations of four different non-model bird lineages (species or species pairs) with different levels of genetic divergence. We find that, in all species, stringent similarity thresholds result in fewer alleles per locus than more liberal thresholds, which appears to be the result of high levels of over-splitting. The frequency of putative under-splitting, conversely, is low at all thresholds. Inferred genetic distances between individuals, gene tree depths, and estimates of the ancestral mutation-scaled effective population size (θ) differ depending upon the similarity threshold applied. Relative differences in inferences across species differ even when the same threshold is applied, but may be dramatically different when datasets assembled under different thresholds are compared. These differences not only complicate comparisons across species, but also preclude the application of standard mutation rates for parameter calibration. We suggest some best practices for assembling short read data to maximize comparability, such as using more liberal thresholds and examining the impact of different thresholds on each dataset.