The latitudinal gradient in rates of evolution for bird beaks, a species interaction trait.

Where is evolution fastest? The biotic interactions hypothesis proposes that greater species richness creates more ecological opportunity, driving faster evolution at low latitudes, whereas the 'empty niches' hypothesis proposes that ecological opportunity is greater where diversity is low, spurring faster evolution at high latitudes. We tested these contrasting predictions by analysing rates of beak evolution for a global dataset of 1141 avian sister species. Rates of beak size evolution are similar across latitudes, with some evidence that beak shape evolves faster in the temperate zone, consistent with the empty niches hypothesis. The empty niches hypothesis is further supported by a meta-analysis showing that rates of trait evolution and recent speciation are generally faster in the temperate zone, whereas rates of molecular evolution are slightly faster in the tropics. Our results suggest that drivers of evolutionary diversification are either similar across latitudes or more potent in the temperate zone, thus calling into question multiple hypotheses that invoke faster tropical evolution to explain the latitudinal diversity gradient.

AVONET: morphological, ecological and geographical data for all birds.

Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.

Faster evolution of a premating reproductive barrier is not associated with faster speciation rates in New World passerine birds.

Why are speciation rates so variable across the tree of life? One hypothesis is that this variation is explained by how rapidly reproductive barriers evolve. We tested this hypothesis by conducting a comparative study of the evolution of bird song, a premating barrier to reproduction. Speciation in birds is typically initiated when geographically isolated (allopatric) populations evolve reproductive barriers. We measured the strength of song as a premating barrier between closely related allopatric populations by conducting 2339 field experiments to measure song discrimination for 175 taxon pairs of allopatric or parapatric New World passerine birds, and estimated recent speciation rates from molecular phylogenies. We found evidence that song discrimination is indeed an important reproductive barrier: taxon pairs with high song discrimination in allopatry did not regularly interbreed in parapatry. However, evolutionary rates of song discrimination were not associated with recent speciation rates. Evolutionary rates of song discrimination were also unrelated to latitude or elevation, but species with innate song (suboscines) evolved song discrimination much faster than species with learned song (oscines). We conclude that song is a key premating reproductive barrier in birds, but faster evolution of this reproductive barrier between populations does not consistently result in faster diversification between species.

Montane species track rising temperatures better in the tropics than in the temperate zone.

Many species are responding to global warming by shifting their distributions upslope to higher elevations, but the observed rates of shifts vary considerably among studies. Here, we test the hypothesis that this variation is in part explained by latitude, with tropical species being particularly responsive to warming temperatures. We analyze two independent empirical datasets-shifts in species' elevational ranges, and changes in composition of forest inventory tree plots. Tropical species are tracking rising temperatures 2.1-2.4 times (range shift dataset) and 10 times (tree plot dataset) better than their temperate counterparts. Models predict that for a 100 m upslope shift in temperature isotherm, species at the equator have shifted their elevational ranges 93-96 m upslope, while species at 45° latitude have shifted only 37-42 m upslope. For tree plots, models predict that a 1°C increase in temperature leads to an increase in community temperature index (CTI), a metric of the average temperature optima of tree species within a plot, of 0.56°C at the equator but no change in CTI at 45° latitude (-0.033°C). This latitudinal gradient in temperature tracking suggests that tropical montane communities may be on an "escalator to extinction" as global temperatures continue to rise.

Evolutionary conservatism will limit responses to climate change in the tropics.

Rapid species turnover in tropical mountains has fascinated biologists for centuries. A popular explanation for this heightened beta diversity is that climatic stability at low latitudes promotes the evolution of narrow thermal tolerance ranges, leading to local adaptation, evolutionary divergence and parapatric speciation along elevational gradients. However, an emerging consensus from research spanning phylogenetics, biogeography and behavioural ecology is that this process rarely, if ever, occurs. Instead, closely related species typically occupy a similar elevational niche, while species with divergent elevational niches tend to be more distantly related. These results suggest populations have responded to past environmental change not by adapting and diverging in place, but instead by shifting their distributions to tightly track climate over time. We argue that tropical species are likely to respond similarly to ongoing and future climate warming, an inference supported by evidence from recent range shifts. In the absence of widespread in situ adaptation to new climate regimes by tropical taxa, conservation planning should prioritize protecting large swaths of habitat to facilitate movement.

Climate change causes upslope shifts and mountaintop extirpations in a tropical bird community.

Montane species worldwide are shifting upslope in response to recent temperature increases. These upslope shifts are predicted to lead to mountaintop extinctions of species that live only near mountain summits, but empirical examples of populations that have disappeared are sparse. We show that recent warming constitutes an "escalator to extinction" for birds on a remote Peruvian mountain-high-elevation species have declined in both range size and abundance, and several previously common mountaintop residents have disappeared from the local community. Our findings support projections that warming will likely drive widespread extirpations and extinctions of high-elevation taxa in the tropical Andes. Such climate change-driven mountaintop extirpations may be more likely in the tropics, where temperature seems to exert a stronger control on species' range limits than in the temperate zone. In contrast, we show that lowland bird species at our study site are expanding in range size as they shift their upper limits upslope and may thus benefit from climate change.

Adaptation and Latitudinal Gradients in Species Interactions: Nest Predation in Birds.

AbstractAre biotic interactions stronger in the tropics? Here, we investigate nest predation in birds, a canonical example of a strong tropical biotic interaction. Counter to expectations, daily rates of nest predation vary minimally with latitude. However, life-history traits that influence nest predation have diverged between latitudes. For example, tropical species have evolved a longer average nesting period, which is associated with reduced rates of nest attendance by parents. Daily nest mortality declines with nesting period length within regions, but tropical species have a higher intercept. Consequently, for the same nesting period length, tropical species experience higher daily nest predation rates than temperate species. The implication of this analysis is that the evolved difference in nesting period length between latitudes produces a flatter latitudinal gradient in daily nest predation than would otherwise be predicted. We propose that adaptation may frequently dampen geographic patterns in interaction rates.

Speciation and gene flow across an elevational gradient in New Guinea kingfishers.

Closely related species with parapatric elevational ranges are ubiquitous in tropical mountains worldwide. The gradient speciation hypothesis proposes that these series are the result of in situ ecological speciation driven by divergent selection across elevation. Direct tests of this scenario have been hampered by the difficulty inferring the geographic arrangement of populations at the time of divergence. In cichlids, sticklebacks and Timema stick insects, support for ecological speciation driven by other selective pressures has come from demonstrating parallel speciation, where divergence proceeds independently across replicated environmental gradients. Here, we take advantage of the unique geography of the island of New Guinea to test for parallel gradient speciation in replicated populations of Syma kingfishers that show extremely subtle differentiation across elevation and between historically isolated mountain ranges. We find that currently described high-elevation and low-elevation species have reciprocally monophyletic gene trees and form nuclear DNA clusters, rejecting this hypothesis. However, demographic modelling suggests selection has likely maintained species boundaries in the face of gene flow following secondary contact. We compile evidence from the published literature to show that although in situ gradient speciation in labile organisms such as birds appears rare, divergent selection and post-speciation gene flow may be an underappreciated force in the origin of elevational series and tropical beta diversity along mountain slopes.

Rapid upslope shifts in New Guinean birds illustrate strong distributional responses of tropical montane species to global warming.

Temperate-zone species have responded to warming temperatures by shifting their distributions poleward and upslope. Thermal tolerance data suggests that tropical species may respond to warming temperatures even more strongly than temperate-zone species, but this prediction has yet to be tested. We addressed this data gap by conducting resurveys to measure distributional responses to temperature increases in the elevational limits of the avifaunas of two geographically and faunally independent New Guinean mountains, Mt. Karimui and Karkar Island, 47 and 44 y after they were originally surveyed. Although species richness is roughly five times greater on mainland Mt. Karimui than oceanic Karkar Island, distributional shifts at both sites were similar: upslope shifts averaged 113 m (Mt. Karimui) and 152 m (Karkar Island) for upper limits and 95 m (Mt. Karimui) and 123 m (Karkar Island) for lower limits. We incorporated these results into a metaanalysis to compare distributional responses of tropical species with those of temperate-zone species, finding that average upslope shifts in tropical montane species match local temperature increases significantly more closely than in temperate-zone montane species. That tropical species appear to be strong responders has global conservation implications and provides empirical support to hitherto untested models that predict widespread extinctions in upper-elevation tropical endemics with small ranges.

Competitive Interactions upon Secondary Contact Drive Elevational Divergence in Tropical Birds.

Tropical mountains harbor exceptionally high biodiversity, which is in part due to the marked elevational stratification of tropical biotas. However, the factors that influence the evolution of elevational distributions remain uncertain. I used a database of sister species of tropical montane birds from 41 families and three regions-the Neotropics, the Himalayas, and New Guinea-to test whether patterns of elevational divergence were consistent with (1) a stochastic process, (2) ecological sorting of elevational divergence that occurred in allopatry, or (3) elevational divergence driven by competitive interactions upon secondary contact. The stochastic and ecological sorting hypotheses predict that increased elevational divergence in sympatric sister species is explained by their greater evolutionary age, whereas the competitive interactions hypothesis predicts that elevational divergence is explained by geographical overlap. I found that genetic distances were unrelated to elevational divergence and that allopatric sister species occupied similar elevational distributions regardless of genetic distance in each region. Instead, sympatry was the only significant predictor of elevational divergence; regardless of evolutionary age, sympatric sister species had greater elevational divergence than allopatric sister species in each region, as predicted by the competitive interactions hypothesis. Importantly, this pattern occurred in all three geographic regions, which suggests that competition-driven elevational divergence upon secondary contact is a general process of community assembly in tropical montane avifaunas.

Response to comment on "Interspecific competition limits bird species' ranges on tropical mountains".

Xing et al. (1) create new variables and fit models to argue against the hypothesis that interspecific competition shapes species' elevational ranges. However, their key newly created variable is best interpreted as a proxy for the important variable of the interspecific competition hypothesis. Thus, their reanalysis uncovers the patterns we already described that are consistent with the interspecific competition hypothesis.

On the predictability of phenotypic divergence in geographic isolation.

Do related populations that are separated by barriers predictably evolve differences from one another over time, or is such divergence idiosyncratic and unpredictable? We test these alternatives by investigating patterns of trait evolution for 54 sister pairs of Andean forest birds that live in similar environments on either side of the arid Marañón Gap, a strong dispersal barrier for humid montane species. We measured divergence in both sexual (song and plumage) and ecological (beak size and beak shape) traits. Sexual traits evolve in a clock-like fashion, with trait divergence positively correlated with genetic distance (r = 0.6-0.7). In contrast, divergence in ecological traits is uncorrelated or only loosely correlated with genetic distance (r = 0.0-0.3). Thus, for geographically isolated Andean montane forest birds that live in similar environments, divergence is predictable in sexual traits, but not for ecological traits. This means that sexual trait divergence occurs independently of adaptive ecological divergence within the mega-diverse tropical Andean avifauna. Last, we show that variation in genetic divergence across a biogeographic barrier is associated with traits that are proxies for species' opportunities for dispersal (low elevation limit and elevational niche breadth), but not with traits that are proxies for species' dispersal abilities (hand-wing index and foraging strata).

Interspecific competition limits bird species' ranges in tropical mountains.

Species' geographic ranges are limited by climate and species interactions. Climate is the prevailing explanation for why species live only within narrow elevational ranges in megadiverse biodiverse tropical mountains, but competition can also restrict species' elevational ranges. We test contrasting predictions of these hypotheses by conducting a global comparative test of birds' elevational range sizes within 31 montane regions, using more than 4.4 million citizen science records from eBird to define species' elevational ranges in each region. We find strong support that competition, not climate, is the leading driver of narrow elevational ranges. These results highlight the importance of species interactions in shaping species' ranges in tropical mountains, Earth's hottest biodiversity hotspots.

The formation of avian montane diversity across barriers and along elevational gradients.

Tropical mountains harbor exceptional concentrations of Earth's biodiversity. In topographically complex landscapes, montane species typically inhabit multiple mountainous regions, but are absent in intervening lowland environments. Here we report a comparative analysis of genome-wide DNA polymorphism data for population pairs from eighteen Indo-Pacific bird species from the Moluccan islands of Buru and Seram and from across the island of New Guinea. We test how barrier strength and relative elevational distribution predict population differentiation, rates of historical gene flow, and changes in effective population sizes through time. We find population differentiation to be consistently and positively correlated with barrier strength and a species' altitudinal floor. Additionally, we find that Pleistocene climate oscillations have had a dramatic influence on the demographics of all species but were most pronounced in regions of smaller geographic area. Surprisingly, even the most divergent taxon pairs at the highest elevations experience gene flow across barriers, implying that dispersal between montane regions is important for the formation of montane assemblages.

The latitudinal taxonomy gradient.

Emerging large-scale datasets coupled with statistical advances have provided new insights into the processes that generate the latitudinal diversity gradient (LDG). But many of these studies run into an old, if often underappreciated, problem: The interpretation of the data critically depends on the consistent application of criteria to define what constitutes a species. This is particularly pernicious for the LDG because good species have been easier to recognize in temperate than in tropical regions. We provide evidence that this latitudinal taxonomy gradient exists, discuss how this potentially impacts inferences about latitudinal variation in ecoevolutionary processes such as population differentiation and speciation, and provide a roadmap for how to mitigate taxonomic biases in the study of biodiversity patterns.

Pelagic fish predation is stronger at temperate latitudes than near the equator.

Species interactions are widely thought to be strongest in the tropics, potentially contributing to the greater number of species at lower latitudes. Yet, empirical tests of this "biotic interactions" hypothesis remain limited and often provide mixed results. Here, we analyze 55 years of catch per unit effort data from pelagic longline fisheries to estimate the strength of predation exerted by large predatory fish in the world's oceans. We test two central tenets of the biotic interactions hypothesis: that predation is (1) strongest near the equator, and (2) positively correlated with species richness. Counter to these predictions, we find that predation is (1) strongest in or near the temperate zone and (2) negatively correlated with oceanic fish species richness. These patterns suggest that, at least for pelagic fish predation, common assumptions about the latitudinal distribution of species interactions do not apply, thereby challenging a leading explanation for the latitudinal gradient in species diversity.

Macroevolutionary convergence connects morphological form to ecological function in birds.

Animals have diversified into a bewildering variety of morphological forms exploiting a complex configuration of trophic niches. Their morphological diversity is widely used as an index of ecosystem function, but the extent to which animal traits predict trophic niches and associated ecological processes is unclear. Here we use the measurements of nine key morphological traits for >99% bird species to show that avian trophic diversity is described by a trait space with four dimensions. The position of species within this space maps with 70-85% accuracy onto major niche axes, including trophic level, dietary resource type and finer-scale variation in foraging behaviour. Phylogenetic analyses reveal that these form-function associations reflect convergence towards predictable trait combinations, indicating that morphological variation is organized into a limited set of dimensions by evolutionary adaptation. Our results establish the minimum dimensionality required for avian functional traits to predict subtle variation in trophic niches and provide a global framework for exploring the origin, function and conservation of bird diversity.

Ecological and geographical overlap drive plumage evolution and mimicry in woodpeckers.

Organismal appearances are shaped by selection from both biotic and abiotic drivers. For example, Gloger's rule describes the pervasive pattern that more pigmented populations are found in more humid areas. However, species may also converge on nearly identical colours and patterns in sympatry, often to avoid predation by mimicking noxious species. Here we leverage a massive global citizen-science database to determine how biotic and abiotic factors act in concert to shape plumage in the world's 230 species of woodpeckers. We find that habitat and climate profoundly influence woodpecker plumage, and we recover support for the generality of Gloger's rule. However, many species exhibit remarkable convergence explained neither by these factors nor by shared ancestry. Instead, this convergence is associated with geographic overlap between species, suggesting occasional strong selection for interspecific mimicry.