The Evolution of Rodent Tail Morphology.

AbstractPopulation-level variation in rodent tail structures has been variously attributed to facilitating social communication, locomotion, thermoregulation, and predator avoidance. Little is known, however, about the applicability of these ecological and social correlates to explaining the tremendous interspecific diversity of this appendage. To investigate the potential drivers of rodent tail morphology at a macroevolutionary level, we first carefully reviewed the literature and constructed a list of major hypotheses regarding this variation. We then compiled a database of 11 different tail traits related to length, color, texture, and ecological characteristics for 2,101 species of rodents (order Rodentia) and examined their key evolutionary correlates. Using Bayesian phylogenetic mixed models across the entire order and additionally within the five rodent suborders, we found that tail length is correlated with both temperature (Allen's rule) and locomotory mode, that black tips are more common in brightly lit environments, that naked tails are often found in warmer climates, that fluffy-tipped tails are more common in smaller and/or arboreal species, that prehensility is predominant in arboreal species and/or species with longer tails, and that tail autotomy is more common in open environments. Most of our tested predictions, largely drawn from population-level studies, are not recapitulated across the entire order, potentially indicating a role of local ecological context in shaping tail morphology.

Anthropogenic nest material use in a global sample of birds.

As humans increasingly modify the natural world, many animals have responded by changing their behaviour. Understanding and predicting the extent of these responses is a key step in conserving these species. For example, the tendency for some species of birds to incorporate anthropogenic items-particularly plastic material-into their nests is of increasing concern, as in some cases, this behaviour has harmful effects on adults, young and eggs. Studies of this phenomenon, however, have to date been largely limited in geographic and taxonomic scope. To investigate the global correlates of anthropogenic (including plastic) nest material use, we used Bayesian phylogenetic mixed models and a data set of recorded nest materials in 6147 species of birds. We find that, after controlling for research effort and proximity to human landscape modifications, anthropogenic nest material use is correlated with synanthropic (artificial) nesting locations, breeding environment and the number of different nest materials the species has been recorded to use. We also demonstrate that body mass, range size, conservation status and brain size do not explain variation in the recorded use of anthropogenic nest materials. These results indicate that anthropogenic materials are more likely to be included in nests when they are more readily available, as well as potentially by species that are more flexible in their nest material choice.

Nest architecture influences host use by avian brood parasites and is shaped by coevolutionary dynamics.

Brood (social) parasites and their hosts exhibit a wide range of adaptations and counter-adaptations as part of their ongoing coevolutionary arms races. Obligate avian brood parasites are expected to use potential host species with more easily accessible nests, while potential hosts are expected to evade parasitism by building more concealed nests that are difficult for parasites to enter and in which to lay eggs. We used phylogenetically informed comparative analyses, a global database of the world's brood parasites, their host species, and the design of avian host and non-host nests (approx. 6200 bird species) to examine first, whether parasites preferentially target host species that build open nests and, second, whether host species that build enclosed nests are more likely to be targeted by specialist parasites. We found that species building more accessible nests are more likely to serve as hosts, while host species with some of the more inaccessible nests are targeted by more specialist brood parasites. Furthermore, evolutionary-transition analyses demonstrate that host species building enclosed nests frequently evolve to become non-hosts. We conclude that nest architecture and the accessibility of nests for parasitism represent a critical stage of the ongoing coevolutionary arms race between avian brood parasites and their hosts.

Limited ecological opportunity influences the tempo of morphological evolution in birds.

According to classic models of lineage diversification and adaptive radiation, phenotypic evolution should accelerate in the context of ecological opportunity and slow down when niches become saturated.1,2 However, only weak support for these ideas has been found in nature, perhaps because most analyses make the biologically unrealistic assumption that clade members contribute equally to reducing ecological opportunity, even when they occur in different continents or specialize on different habitats and diets. To view this problem through a different lens, we adapted a new phylogenetic modeling approach that accounts for the fact that competition for ecological opportunity only occurs between species that coexist and share similar habitats and diets. Applying this method to trait data for nearly all extant species of landbirds,3 we find a widespread signature of decelerating trait evolution in lineages adapted to similar habitats or diets. The strength of this pattern was consistent across latitudes when comparing tropical and temperate assemblages. Our results provide little support for the idea that increased diversity and tighter packing of niches accentuates evolutionary slowdowns in the tropics and instead suggest that limited ecological opportunity can be an important factor determining the rate of morphological diversification at a global scale.

The macroevolutionary dynamics of mammalian sexual size dimorphism.

Sexual size dimorphism (SSD) is a common phenomenon across the animal kingdom. Mammals are unusual in primarily displaying male-biased SSD, where males of a species are typically larger than females. The driving factors behind the evolution of this SSD have been much debated, with popular hypotheses invoking the influence of mating system and social organization via sexual selection, dietary niche divergence and broad-scale correlations with body size (Rensch's rule). Here, we investigate the macroevolutionary origins and maintenance of SSD among mammals, using phylogenetic general mixed linear models and a comprehensive global dataset to evaluate correlations of diet, body mass, seasonality, social organization and mating system with SSD type. We find that SSD as a whole is lost at a greater rate than it is gained, with female-biased SSD being particularly unstable. Non-monogamous mating systems, vertebrate prey consumption and temperature seasonality correlate with male-biased SSD, while polyandry correlates with female-biased SSD, and both types of SSD are positively correlated with body mass. This is in partial contrast to the predictions of Rensch's rule, which predicts that female-biased SSD would correlate negatively with body size. Taken together, our results highlight the importance of considering multiple ecological and social drivers when evaluating the macroevolutionary trajectory of sex differences in body size.

Beak shape and nest material use in birds.

The evolution of behaviour can both influence, and be influenced by, morphology. Recent advances in methods and data availability have facilitated broad-scale investigations of physical form and behavioural function in many contexts, but the relationship between animal morphology and object manipulation-particularly objects used in construction-remains largely unknown. Here, we employ a new global database of nest materials used by 5924 species of birds together with phylogenetically informed random forest models to evaluate the link between beak shape and these nest-building materials. We find that beak morphology, together with species diet and access to materials, can predict nest-material use above chance and with high accuracy (68-97%). Much of this relationship, however, is driven by phylogenetic signal and sampling biases. We therefore conclude that while variation in nest material use is linked with that of beak shape across bird species, these correlations are modulated by the ecological context and evolutionary history of these species. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Evolution of nest architecture in tyrant flycatchers and allies.

Innovations in nest design are thought to be one potential factor in the evolutionary success of passerine birds (order: Passeriformes), which colonized new ecological niches as they diversified in the Oligocene and Miocene. In particular, tyrant flycatchers and their allies (parvorder: Tyrannida) are an extremely diverse group of New World suboscine passerines occupying a wide range of habitats and exhibiting substantial extant variation in nest design. To explore the evolution of nest architecture in this clade, we first described nest traits across the Tyrannida phylogeny and estimated ancestral nest conditions. We then quantified macroevolutionary transition rates between nest types, examined a potential coevolutionary relationship between nest type and habitat, and used phylogenetic mixed models to determine possible ecological and environmental correlates of nest design. The Tyrannida ancestor probably built a cup nest in a closed habitat, and dome nests independently evolved at least 15 times within this group. Both cup- and dome-nesting species diversified into semi-open and open habitats, and we did not detect a coevolutionary relationship between nest type and habitat. Furthermore, nest type was not significantly correlated with several key ecological, life-history and environmental traits, suggesting that broad variation in Tyrannida nest architecture may not easily be explained by a single factor. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Kinbank: A global database of kinship terminology.

For a single species, human kinship organization is both remarkably diverse and strikingly organized. Kinship terminology is the structured vocabulary used to classify, refer to, and address relatives and family. Diversity in kinship terminology has been analyzed by anthropologists for over 150 years, although recurrent patterning across cultures remains incompletely explained. Despite the wealth of kinship data in the anthropological record, comparative studies of kinship terminology are hindered by data accessibility. Here we present Kinbank, a new database of 210,903 kinterms from a global sample of 1,229 spoken languages. Using open-access and transparent data provenance, Kinbank offers an extensible resource for kinship terminology, enabling researchers to explore the rich diversity of human family organization and to test longstanding hypotheses about the origins and drivers of recurrent patterns. We illustrate our contribution with two examples. We demonstrate strong gender bias in the phonological structure of parent terms across 1,022 languages, and we show that there is no evidence for a coevolutionary relationship between cross-cousin marriage and bifurcate-merging terminology in Bantu languages. Analysing kinship data is notoriously challenging; Kinbank aims to eliminate data accessibility issues from that challenge and provide a platform to build an interdisciplinary understanding of kinship.

Global drivers of variation in cup nest size in passerine birds.

The size of a bird's nest can play a key role in ensuring reproductive success and is determined by a variety of factors. The primary function of the nest is to protect offspring from the environment and predators. Field studies in a number of passerine species have indicated that higher-latitude populations in colder habitats build larger nests with thicker walls compared to lower-latitude populations, but that these larger nests are more vulnerable to predation. Increases in nest size can also be driven by sexual selection, as nest size can act as a signal of parental quality and prompt differential investment in other aspects of care. It is unknown, however, how these microevolutionary patterns translate to a macroevolutionary scale. Here, we investigate potential drivers of variation in the outer and inner volume of open cup nests using a large dataset of nest measurements from 1117 species of passerines breeding in a diverse range of environments. Our dataset is sourced primarily from the nest specimens at the Natural History Museum (UK), complemented with information from ornithological handbooks and online databases. We use phylogenetic comparative methods to test long-standing hypotheses about potential macroevolutionary correlates of nest size, namely nest location, clutch size and variables relating to parental care, together with environmental and geographical factors such as temperature, rainfall, latitude and insularity. After controlling for phylogeny and parental body size, we demonstrate that the outer volume of the nest is greater in colder climates, in island-dwelling species and in species that nest on cliffs or rocks. By contrast, the inner cup volume is associated solely with average clutch size, increasing with the number of chicks raised in the nest. We do not find evidence that nest size is related to the length of parental care for nestlings. Our study reveals that the average temperature in the breeding range, along with several key life-history traits and proxies of predation threat, shapes the global interspecific variation in passerine cup nest size. We also showcase the utility of museum nest collections-a historically underused resource-for large-scale studies of trait evolution.

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.

Aposematism in mammals.

Aposematic coloration is traditionally considered to signal unpalatability or toxicity. In mammals, most research has focused on just one form of defense, namely, noxious anal secretions, and its black-and-white advertisement as exemplified by skunks. The original formulation of aposematism, however, encompassed a broader range of morphological, physiological, and behavioral defenses, and there are many mammal species with black-and-white contrasting patterns that do not have noxious adaptations. Here, using Bayesian phylogenetic models and data from 1726 terrestrial nonvolant mammals we find that two aspects of conspicuous coloration, black-and-white coloration patterns on the head and body, advertise defenses that are morphological (spines, large body size), behavioral (pugnacity), and physiological (anal secretions), as well as being involved with sexual signaling and environmental factors linked to crypsis. Within Carnivora, defensive anal secretions are associated with complex black-and-white head patterns and longitudinal black-and-white body striping; in primates, larger bodied species exhibit irregular patches of black-and-white pelage; and in rodents, pugnacity is linked to sharp countershading and irregular blocks of white and black pelage. We show that black-and-white coloration in mammals is multifunctional, that it serves to warn predators of several defenses other than noxious anal secretions, and that aposematism in mammals is not restricted to carnivores.

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.

Erratum: Pama-Nyungan grandparent systems change with grandchildren, but not cross-cousin terms or social norms.

[This corrects the article DOI: 10.1017/ehs.2020.31.].

Ecological drivers of global gradients in avian dispersal inferred from wing morphology.

An organism's ability to disperse influences many fundamental processes, from speciation and geographical range expansion to community assembly. However, the patterns and underlying drivers of variation in dispersal across species remain unclear, partly because standardised estimates of dispersal ability are rarely available. Here we present a global dataset of avian hand-wing index (HWI), an estimate of wing shape widely adopted as a proxy for dispersal ability in birds. We show that HWI is correlated with geography and ecology across 10,338 (>99%) species, increasing at higher latitudes and with migration, and decreasing with territoriality. After controlling for these effects, the strongest predictor of HWI is temperature variability (seasonality), with secondary effects of diet and habitat type. Finally, we also show that HWI is a strong predictor of geographical range size. Our analyses reveal a prominent latitudinal gradient in HWI shaped by a combination of environmental and behavioural factors, and also provide a global index of avian dispersal ability for use in community ecology, macroecology, and macroevolution.

Ecology and allometry predict the evolution of avian developmental durations.

The duration of the developmental period represents a fundamental axis of life-history variation, yet broad insights regarding the drivers of this diversity are currently lacking. Here, we test mechanistic and ecological explanations for the evolution of developmental duration using embryological data and information on incubation and fledging for 3096 avian species. Developmental phases associated primarily with growth are the longest and most variable, consistent with a role for allometric constraint in determining the duration of development. In addition, developmental durations retain a strong imprint of deep evolutionary history and body size differences among species explain less variation than previously thought. Finally, we reveal ecological correlates of developmental durations, including variables associated with the relative safety of the developmental environment and pressures of breeding phenology. Overall, our results provide broad-scale insight into the relative importance of mechanistic, ecological and evolutionary constraints in shaping the diversification of this key life-history trait.

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.

Pama-Nyungan grandparent systems change with grandchildren, but not cross-cousin terms or social norms.

Kinship is a fundamental and universal aspect of the structure of human society. The kinship category of 'grandparents' is socially salient, due to grandparents' investment in the care of the grandchildren as well as to older generations' control of wealth and cultural knowledge, but the evolutionary dynamics of grandparent terms has yet to be studied in a phylogenetically explicit context. Here, we present the first phylogenetic comparative study of grandparent terms by investigating 134 languages in Pama-Nyungan, an Australian family of hunter-gatherer languages. We infer that proto-Pama-Nyungan had, with high certainty, four separate terms for grandparents. This state then shifted into either a two-term system that distinguishes the genders of the grandparents or a three-term system that merges the 'parallel' grandparents, which could then transition into a different three-term system that merges the 'cross' grandparents. We find no support for the co-evolution of these systems with either community marriage organisation or post-marital residence. We find some evidence for the correlation of grandparent and grandchild terms, but no support for the correlation of grandparent and cross-cousin terms, suggesting that grandparents and grandchildren potentially form a single lexical category but that the entire kinship system does not necessarily change synchronously.

Usage frequency and lexical class determine the evolution of kinship terms in Indo-European.

Languages do not replace their vocabularies at an even rate: words endure longer if they are used more frequently. This effect, which has parallels in evolutionary biology, has been demonstrated for the core vocabulary, a set of common, unrelated meanings. The extent to which it replicates in closed lexical classes remains to be seen, and may indicate how general this effect is in language change. Here, we use phylogenetic comparative methods to investigate the history of 10 kinship categories, a type of closed lexical class of content words, across 47 Indo-European languages. We find that their rate of replacement is correlated with their usage frequency, and this relationship is stronger than in the case of the core vocabulary, even though the envelope of variation is comparable across the two cases. We also find that the residual variation in the rate of replacement of kinship terms is related to genealogical distance of referent to kin. We argue that this relationship is the result of social changes and corresponding shifts in the entire semantic class of kinship terms, shifts typically not present in the core vocabulary. Thus, an understanding of the scope and limits of social change is needed to understand changes in kinship systems, and broader context is necessary to model cultural evolution in particular and the process of system change in general.

The macroecological dynamics of species coexistence in birds.

Ecological communities are assembled from the overlapping of species in geographic space, but the mechanisms facilitating or limiting such overlaps are difficult to resolve. Here, we combine phylogenetic, morphological and environmental data to model how multiple processes regulate the origin and maintenance of geographic range overlap across 1,115 pairs of avian sister species globally. We show that coexistence cannot be adequately predicted by either dispersal-assembly (that is, biogeographic) models or niche-assembly models alone. Instead, our results overwhelmingly support an integrated model with different assembly processes dominating at different stages of coexistence. The initial attainment of narrow geographic overlap is dictated by intrinsic dispersal ability and the time available for dispersal, whereas wider coexistence is largely dependent on niche availability, increasing with ecosystem productivity and divergence in niche-related traits, and apparently declining as communities become saturated with species. Furthermore, although coexistence of any individual pair of species is highly stochastic, we find that integrating assembly processes allows broad variation in the incidence and extent of coexistence to be predicted with reasonable accuracy. Our findings demonstrate how phylogenetic data coupled with environmental factors and functional traits can begin to clarify the multi-layered processes shaping the distribution of biodiversity at large spatial scales.

Tempo and timing of ecological trait divergence in bird speciation.

Organismal traits may evolve either gradually or in rapid pulses, but the relative importance of these modes in the generation of species differences is unclear. Additionally, while pulsed evolution is frequently assumed to be associated with speciation events, few studies have explicitly examined how the tempo of trait divergence varies with respect to different geographical phases of speciation, starting with geographic isolation and ending, in many cases, with spatial overlap (sympatry). Here we address these issues by combining divergence time estimates, trait measurements and geographic range data for 952 avian sister species pairs worldwide to examine the tempo and timing of trait divergence in recent speciation events. We show that patterns of divergence in key ecological traits are not gradual, but instead seem to follow a pattern of relative stasis interspersed with evolutionary pulses of varying magnitude. We also find evidence that evolutionary pulses generally precede sympatry, and that greater trait disparity is associated with sympatry. These findings suggest that early pulses of trait divergence promote subsequent transitions to sympatry, rather than occurring after sympatry has been established. Incorporating models with evolutionary pulses of varying magnitude into speciation theory may explain why some species pairs achieve rapid sympatry whereas others undergo prolonged geographical exclusion.