Complexity of avian evolution revealed by family-level genomes.

Despite tremendous efforts in the past decades, relationships among main avian lineages remain heavily debated without a clear resolution. Discrepancies have been attributed to diversity of species sampled, phylogenetic method and the choice of genomic regions1-3. Here we address these issues by analysing the genomes of 363 bird species4 (218 taxonomic families, 92% of total). Using intergenic regions and coalescent methods, we present a well-supported tree but also a marked degree of discordance. The tree confirms that Neoaves experienced rapid radiation at or near the Cretaceous-Palaeogene boundary. Sufficient loci rather than extensive taxon sampling were more effective in resolving difficult nodes. Remaining recalcitrant nodes involve species that are a challenge to model due to either extreme DNA composition, variable substitution rates, incomplete lineage sorting or complex evolutionary events such as ancient hybridization. Assessment of the effects of different genomic partitions showed high heterogeneity across the genome. We discovered sharp increases in effective population size, substitution rates and relative brain size following the Cretaceous-Palaeogene extinction event, supporting the hypothesis that emerging ecological opportunities catalysed the diversification of modern birds. The resulting phylogenetic estimate offers fresh insights into the rapid radiation of modern birds and provides a taxon-rich backbone tree for future comparative studies.

Thresholds for adding degraded tropical forest to the conservation estate.

Logged and disturbed forests are often viewed as degraded and depauperate environments compared with primary forest. However, they are dynamic ecosystems1 that provide refugia for large amounts of biodiversity2,3, so we cannot afford to underestimate their conservation value4. Here we present empirically defined thresholds for categorizing the conservation value of logged forests, using one of the most comprehensive assessments of taxon responses to habitat degradation in any tropical forest environment. We analysed the impact of logging intensity on the individual occurrence patterns of 1,681 taxa belonging to 86 taxonomic orders and 126 functional groups in Sabah, Malaysia. Our results demonstrate the existence of two conservation-relevant thresholds. First, lightly logged forests (<29% biomass removal) retain high conservation value and a largely intact functional composition, and are therefore likely to recover their pre-logging values if allowed to undergo natural regeneration. Second, the most extreme impacts occur in heavily degraded forests with more than two-thirds (>68%) of their biomass removed, and these are likely to require more expensive measures to recover their biodiversity value. Overall, our data confirm that primary forests are irreplaceable5, but they also reinforce the message that logged forests retain considerable conservation value that should not be overlooked.

Changes in the functional diversity of modern bird species over the last million years.

Despite evidence of declining biosphere integrity, we currently lack understanding of how the functional diversity associated with changes in abundance among ecological communities has varied over time and before widespread human disturbances. We combine morphological, ecological, and life-history trait data for >260 extant bird species with genomic-based estimates of changing effective population size (Ne) to quantify demographic-based shifts in avian functional diversity over the past million years and under pre-anthropogenic climate warming. We show that functional diversity was relatively stable over this period, but underwent significant changes in some key areas of trait space due to changing species abundances. Our results suggest that patterns of population decline over the Pleistocene have been concentrated in particular regions of trait space associated with extreme reproductive strategies and low dispersal ability, consistent with an overall erosion of functional diversity. Further, species most sensitive to climate warming occupied a relatively narrow region of functional space, indicating that the largest potential population increases and decreases under climate change will occur among species with relatively similar trait sets. Overall, our results identify fluctuations in functional space of extant species over evolutionary timescales and represent the demographic-based vulnerability of different regions of functional space among these taxa. The integration of paleodemographic dynamics with functional trait data enhances our ability to quantify losses of biosphere integrity before anthropogenic disturbances and attribute contemporary biodiversity loss to different drivers over time.

Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation.

Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by two descendant species. This assumption contrasts with models of speciation at a micro-evolutionary scale where descendants' phenotypic distributions are sub-samples of the ancestral distribution. Different speciation mechanisms can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of ancestral phenotypic distribution at speciation. Here we develop an Asymmetric Brownian Motion model (ABM) that relaxes the assumption of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also infers the mode of phenotypic inheritance at speciation, which can range from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.

Disentangling the drivers of urban bird diversity in the non-breeding season: A general synthesis.

Current knowledge about the impacts of urbanisation on bird assemblages is based on evidence from studies partly or wholly undertaken in the breeding season. In comparison, the non-breeding season remains little studied, despite the fact that winter conditions at higher latitudes are changing more rapidly than other seasons. During the non-breeding season, cities may attract or retain bird species because they offer milder conditions or better feeding opportunities than surrounding habitats. However, the range of climatic, ecological and anthropogenic mechanisms shaping different facets of urban bird diversity in the non-breeding season are poorly understood. We explored these mechanisms using structural equation modelling to assess how urbanisation affects the taxonomic, phylogenetic and functional diversity of avian assemblages sampled worldwide in the non-breeding season. We found that minimum temperature, elevation, urban area and city age played a critical role in determining taxonomic diversity while a range of factors-including productivity, precipitation, elevation, distance to coasts and rivers, socio-economic (as a proxy of human facilitation) and road density-each contributed to patterns of phylogenetic and functional diversity. The structure and function of urban bird assemblages appear to be predominantly shaped by temperature, productivity and city age, with effects of these factors differing across seasons. Our results underline the importance of considering multiple hypotheses, including seasonal effects, when evaluating the impacts of urbanisation on biodiversity.

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.

Unravelling the complexities of biotic homogenization and heterogenization in the British avifauna.

Biotic homogenization is a process whereby species assemblages become more similar through time. The standard way of identifying the process of biotic homogenization is to look for decreases in spatial beta-diversity. However, using a single assemblage-level metric to assess homogenization can mask important changes in the occupancy patterns of individual species. Here, we analysed changes in the spatial beta-diversity patterns (i.e. biotic heterogenization or homogenization) of British bird assemblages within 30 km × 30 km regions between two periods (1988-1991 and 2008-2011). We partitioned the change in spatial beta-diversity into extirpation and colonization-resultant change (i.e. change in spatial beta-diversity within each region resulting from both extirpation and colonization). We used measures of abiotic change in combination with Bayesian modelling to disentangle the drivers of biotic heterogenization and homogenization. We detected both heterogenization and homogenization across the two time periods and three measures of diversity (taxonomic, phylogenetic, and functional). In addition, both extirpation and colonization contributed to the observed changes, with heterogenization mainly driven by extirpation and homogenization by colonization. These assemblage-level changes were primarily due to shifting occupancy patterns of generalist species. Compared to habitat generalists, habitat specialists had significantly (i) higher average contributions to colonization-resultant change (indicating heterogenization within a region due to colonization) and (ii) lower average contributions to extirpation-resultant change (indicating homogenization from extirpation). Generalists showed the opposite pattern. Increased extirpation-resultant homogenization within regions was associated with increased urban land cover and decreased habitat diversity, precipitation, and temperature. Changes in extirpation-resultant heterogenization and colonization-resultant heterogenization were associated with differences in elevation between regions and changes in temperature and land cover. Many of the 'winners' (i.e. species that increased in occupancy) were species that had benefitted from conservation action (e.g. buzzard (Buteo buteo)). The 'losers' (i.e. those that decreased in occupancy) consisted primarily of previously common species, such as cuckoo (Cuculus canorus). Our results show that focusing purely on changes in spatial beta-diversity over time may obscure important information about how changes in the occupancy patterns of individual species contribute to homogenization and heterogenization.

Corrigendum: Reductions in global biodiversity loss predicted from conservation spending.

This corrects the article DOI: 10.1038/nature24295.

A global analysis of avian island diversity-area relationships in the Anthropocene.

Research on island species-area relationships (ISAR) has expanded to incorporate functional (IFDAR) and phylogenetic (IPDAR) diversity. However, relative to the ISAR, we know little about IFDARs and IPDARs, and lack synthetic global analyses of variation in form of these three categories of island diversity-area relationship (IDAR). Here, we undertake the first comparative evaluation of IDARs at the global scale using 51 avian archipelagic data sets representing true and habitat islands. Using null models, we explore how richness-corrected functional and phylogenetic diversity scale with island area. We also provide the largest global assessment of the impacts of species introductions and extinctions on the IDAR. Results show that increasing richness with area is the primary driver of the (non-richness corrected) IPDAR and IFDAR for many data sets. However, for several archipelagos, richness-corrected functional and phylogenetic diversity changes linearly with island area, suggesting that the dominant community assembly processes shift along the island area gradient. We also find that archipelagos with the steepest ISARs exhibit the biggest differences in slope between IDARs, indicating increased functional and phylogenetic redundancy on larger islands in these archipelagos. In several cases introduced species seem to have 're-calibrated' the IDARs such that they resemble the historic period prior to recent extinctions.

What Can Evolutionary History Tell Us about the Functioning of Ecological Communities? The ASN Presidential Debate.

AbstractIn January 2018, Sharon Strauss, then president of the American Society of Naturalists, organized a debate on the following topic: does evolutionary history inform the current functioning of ecological communities? The debaters-Ives, Lau, Mayfield, and Tobias-presented pro and con arguments, caricatured in standard debating format. Numerous examples show that both recent microevolutionary and longer-term macroevolutionary history are important to the ecological functioning of communities. On the other hand, many other examples illustrate that the evolutionary history of communities or community members does not influence ecological function, or at least not very much. This article aims to provide a provocative discussion of the consistent and conflicting patterns that emerge in the study of contemporary and historical evolutionary influences on community function, as well as to identify questions for further study. It is intended as a thought-provoking exercise to explore this complex field, specifically addressing (1) key assumptions and how they can lead us astray and (2) issues that need additional study. The debaters all agree that evolutionary history can inform us about at least some aspects of community function. The underlying question at the root of the debate, however, is how the fields of ecology and evolution can most profitably collaborate to provide a deeper and broader understanding of ecological communities.

Reductions in global biodiversity loss predicted from conservation spending.

Halting global biodiversity loss is central to the Convention on Biological Diversity and United Nations Sustainable Development Goals, but success to date has been very limited. A critical determinant of success in achieving these goals is the financing that is committed to maintaining biodiversity; however, financing decisions are hindered by considerable uncertainty over the likely impact of any conservation investment. For greater effectiveness, we need an evidence-based model that shows how conservation spending quantitatively reduces the rate of biodiversity loss. Here we demonstrate such a model, and empirically quantify how conservation investment reduced biodiversity loss in 109 countries (signatories to the Convention on Biological Diversity and Sustainable Development Goals), by a median average of 29% per country between 1996 and 2008. We also show that biodiversity changes in signatory countries can be predicted with high accuracy, using a dual model that balances the effects of conservation investment against those of economic, agricultural and population growth (human development pressures). Decision-makers can use this model to forecast the improvement that any proposed biodiversity budget would achieve under various scenarios of human development pressure, and then compare these forecasts to any chosen policy target. We find that the impact of spending decreases as human development pressures grow, which implies that funding may need to increase over time. The model offers a flexible tool for balancing the Sustainable Development Goals of human development and maintaining biodiversity, by predicting the dynamic changes in conservation finance that will be needed as human development proceeds.

The causes and ecological context of rapid morphological evolution in birds.

Episodic pulses in morphological diversification are a prominent feature of evolutionary history, driven by factors that remain widely disputed. Resolving this question has proved challenging because comprehensive species-level data are generally unavailable at sufficient scale. Combining global phylogenetic and morphological data for birds, we show that pulses of diversification in lineages and traits tend to occur independently and in different contexts. Speciation pulses are preceded by greater differentiation in overall morphology and habitat niche, then followed by increased rates of beak evolution. Contrary to standard hypotheses, pulses of morphological diversification tend to be associated with habitat niche stability rather than adaptation to different diets and habitat types. These patterns suggest that the timing of diversification varies across traits according to their ecological function, and that pulses of morphological evolution may occur when successful lineages subdivide niche space within particular habitat types. Our results highlight the growing potential of functional trait data sets to refine macroevolutionary models.

Diversity and extinction risk are inversely related at a global scale.

Increases in biodiversity often lead to greater, and less variable, levels of ecosystem functioning. However, whether species are less likely to go extinct in more diverse ecosystems is unclear. We use comprehensive estimates of avian taxonomic, phylogenetic and functional diversity to characterise the global relationship between multiple dimensions of diversity and extinction risk in birds, focusing on contemporary threat status and latent extinction risk. We find that more diverse assemblages have lower mean IUCN threat status despite being composed of species with attributes that make them more vulnerable to extinction, such as large body size or small range size. Indeed, the reduction in current threat status associated with greater diversity far outweighs the increased risk associated with the accumulation of extinction-prone species in more diverse assemblages. Our results suggest that high diversity reduces extinction risk, and that species conservation targets may therefore best be achieved by maintaining high levels of overall biodiversity in natural ecosystems.

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.

A test of Darwin's naturalization conundrum in birds reveals enhanced invasion success in the presence of close relatives.

Biological invasions pose one of the most severe environmental challenges of the twenty-first century. A longstanding idea is that invasion risk is predictable based on the phylogenetic distance - and hence ecological resemblance - between non-native and native species. However, current evidence is contradictory. To explain these mixed results, it has been proposed that the effect is scale-dependent, with invasion inhibited by phylogenetic similarity at small spatial scales but enhanced at larger scales. Analyzing invasion outcomes in a global sample of bird communities, we find no evidence to support this hypothesis. Instead, our results suggest that invaders are locally more successful in the presence of closely related and ecologically similar species, at least in human-altered environments where the majority of invasions have occurred. Functional trait analyses further confirm that the ecological niches of invaders are phylogenetically conserved, supporting the notion that successful invasion in the presence of close relatives is driven by shared adaptations to the types of niches available in novel environments.

Global plant-frugivore trait matching is shaped by climate and biogeographic history.

Species interactions are influenced by the trait structure of local multi-trophic communities. However, it remains unclear whether mutualistic interactions in particular can drive trait patterns at the global scale, where climatic constraints and biogeographic processes gain importance. Here we evaluate global relationships between traits of frugivorous birds and palms (Arecaceae), and how these relationships are affected, directly or indirectly, by assemblage richness, climate and biogeographic history. We leverage a new and expanded gape size dataset for nearly all avian frugivores, and find a positive relationship between gape size and fruit size, that is, trait matching, which is influenced indirectly by palm richness and climate. We also uncover a latitudinal gradient in trait matching strength, which increases towards the tropics and varies among zoogeographic realms. Taken together, our results suggest trophic interactions have consistent influences on trait structure, but that abiotic, biogeographic and richness effects also play important, though sometimes indirect, roles in shaping the functional biogeography of mutualisms.

Global impacts of climate change on avian functional diversity.

Climate change is predicted to drive geographical range shifts, leading to fluctuations in species richness (SR) worldwide. However, the effect of these changes on functional diversity (FD) remains unclear, in part because comprehensive species-level trait data are generally lacking at global scales. Here, we use morphometric and ecological traits for 8268 bird species to estimate the impact of climate change on avian FD. We show that future bird assemblages are likely to undergo substantial shifts in trait structure, with a magnitude of change greater than predicted from SR alone, and a direction of change varying according to geographical location and trophic guild. For example, our models predict that FD of insect predators will increase at higher latitudes with concurrent losses at mid-latitudes, whereas FD of seed dispersing birds will fluctuate across the tropics. Our findings highlight the potential for climate change to drive continental-scale shifts in avian FD with implications for ecosystem function and resilience.

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.

Bird lineages colonizing urban habitats have diversified at high rates across deep time.

Aim: Urbanization exposes species to novel ecological conditions. Some species thrive in urban areas, whereas many others are excluded from these human-made environments. Previous analyses suggest that the ability to cope with rapid environmental change is associated with long-term patterns of diversification, but whether the suite of traits associated with the ability to colonize urban environments is linked to this process remains poorly understood. Location: World. Time period: Current. Major taxa studied: Passerine birds. Methods: We applied macroevolutionary models to a large dataset of passerine birds to compare the evolutionary history of urban-tolerant species with that of urban-avoidant species. Specifically, we examined models of state-dependent speciation and extinction to assess the macroevolution of urban tolerance as a binary trait, in addition to models of quantitative trait-dependent diversification based on relative urban abundance. We also ran simulation-based model assessments to explore potential sources of bias. Results: We provide evidence that historically, species with traits promoting urban colonization have undergone faster diversification than urban-avoidant species, indicating that urbanization favours clades with a historical tendency towards rapid speciation or reduced extinction. In addition, we find that past transitions towards states that currently impede urban colonization by passerines have been more frequent than in the opposite direction. Furthermore, we find a portion of urban-avoidant passerines to be recent and to undergo fast diversification. All highly supported models give this result consistently. Main conclusions: Urbanization is mainly associated with the loss of lineages that are inherently more vulnerable to extinction over deep time, whereas cities tend to be colonized by less vulnerable lineages, for which urbanization might be neutral or positive in terms of longer-term diversification. Urban avoidance is associated with high rates of recent diversification for some clades occurring in regions with relatively intact natural ecosystems and low current levels of urbanization.

Contrasting impacts of competition on ecological and social trait evolution in songbirds.

Competition between closely related species has long been viewed as a powerful selective force that drives trait diversification, thereby generating phenotypic diversity over macroevolutionary timescales. However, although the impact of interspecific competition has been documented in a handful of iconic insular radiations, most previous studies have focused on traits involved in resource use, and few have examined the role of competition across large, continental radiations. Thus, the extent to which broad-scale patterns of phenotypic diversity are shaped by competition remain largely unclear, particularly for social traits. Here, we estimate the effect of competition between interacting lineages by applying new phylogenetic models that account for such interactions to an exceptionally complete dataset of resource-use traits and social signaling traits for the entire radiation of tanagers (Aves, Thraupidae), the largest family of songbirds. We find that interspecific competition strongly influences the evolution of traits involved in resource use, with a weaker effect on plumage signals, and very little effect on song. Our results provide compelling evidence that interspecific exploitative competition contributes to ecological trait diversification among coexisting species, even in a large continental radiation. In comparison, signal traits mediating mate choice and social competition seem to diversify under different evolutionary models, including rapid diversification in the allopatric stage of speciation.