Museomics help resolving the phylogeny of snowfinches (Aves, Passeridae, Montifringilla and allies).

Historical specimens from museum collections provide a valuable source of material also from remote areas or regions of conflict that are not easily accessible to scientists today. With this study, we are providing a taxon-complete phylogeny of snowfinches using historical DNA from whole skins of an endemic species from Afghanistan, the Afghan snowfinch, Pyrgilauda theresae. To resolve the strong conflict between previous phylogenetic hypotheses, we generated novel mitogenome sequences for selected taxa and genome-wide SNP data using ddRAD sequencing for all extant snowfinch species endemic to the Qinghai-Tibet Plateau (QTP) and for an extended intraspecific sampling of the sole Central and Western Palearctic snowfinch species (Montifringilla nivalis). Our phylogenetic reconstructions unanimously refuted the previously suggested paraphyly of genus Pyrgilauda. Misplacement of one species-level taxon (Onychostruthus tazcanowskii) in previous snowfinch phylogenies was undoubtedly inferred from chimeric mitogenomes that included heterospecific sequence information. Furthermore, comparison of novel and previously generated sequence data showed that the presumed sister-group relationship between M. nivalis and the QTP endemic M. henrici was suggested based on flawed taxonomy. Our phylogenetic reconstructions based on genome-wide SNP data and on mitogenomes were largely congruent and supported reciprocal monophyly of genera Montifringilla and Pyrgilauda with monotypic Onychostruthus being sister to the latter. The Afghan endemic P. theresae likely originated from a rather ancient Pliocene out-of-Tibet dispersal probably from a common ancestor with P. ruficollis. Our extended trans-Palearctic sampling for the white-winged snowfinch, M. nivalis, confirmed strong lineage divergence between an Asian and a European clade dated to 1.5 - 2.7 million years ago (mya). Genome-wide SNP data suggested subtle divergence among European samples from the Alps and from the Cantabrian mountains.

Spatio-temporal variation in the wintering associations of an alpine bird.

Many animals make behavioural changes to cope with winter conditions, being gregariousness a common strategy. Several factors have been invoked to explain why gregariousness may evolve during winter, with individuals coming together and separating as they trade off the different costs and benefits of living in groups. These trade-offs may, however, change over space and time as a response to varying environmental conditions. Despite its importance, little is known about the factors triggering gregarious behaviour during winter and its change in response to variation in weather conditions is poorly documented. Here, we aimed at quantifying large-scale patterns in wintering associations over 23 years of the white-winged snowfinch Montifringilla nivalis nivalis. We found that individuals gather in larger groups at sites with harsh wintering conditions. Individuals at colder sites reunite later and separate earlier in the season than at warmer sites. However, the magnitude and phenology of wintering associations are ruled by changes in weather conditions. When the temperature increased or the levels of precipitation decreased, group size substantially decreased, and individuals stayed united in groups for a shorter time. These results shed light on factors driving gregariousness and points to shifting winter climate as an important factor influencing this behaviour.

Ecological and evolutionary drivers of the elevational gradient of diversity.

Ecological, evolutionary, spatial and neutral theories make distinct predictions and provide distinct explanations for the mechanisms that control the relationship between diversity and the environment. Here, we test predictions of the elevational diversity gradient focusing on Iberian bumblebees, grasshoppers and birds. Processes mediated by local abundance and regional diversity concur in explaining local diversity patterns along elevation. Effects expressed through variation in abundance were similar among taxa and point to the overriding role of a physical factor, temperature. This determines how energy is distributed among individuals and ultimately how the resulting pattern of abundance affects species incidence. Effects expressed through variation in regional species pools depended instead on taxon-specific evolutionary history, and lead to diverging responses under similar environmental pressures. Local filters and regional variation also explain functional diversity gradients, in line with results from species richness that indicate an (local) ecological and (regional) historical unfolding of diversity-elevation relationships.

Abiotic, biotic, and evolutionary control of the distribution of C and N isotopes in food webs.

Ecosystem functioning depends on nutrient cycles and their responses to abiotic and biotic determinants, with the influence of evolutionary legacies being generally overlooked in ecosystem ecology. Along a broad elevation gradient characterized by shifting climatic and grazing environments, we addressed clines of plant N and C∶N content and of δ(13)C and δ(15)N in producers (herbs) and in primary (grasshoppers) and secondary (birds) consumers, both within and between species in phylogenetically controlled scenarios. We found parallel and significant intra- and interspecific trends of isotopic variation with elevation in the three groups. In primary producers, nutrient and isotope distributions had a detectable phylogenetic signal that constrained their variation along the environmental gradient. The influence of the environment could not be ascribed to any single factor, and both grazing and climate had an effect on leaf stoichiometry and, thus, on the resources available to consumers. Trends in consumers matched those in plants but often became nonsignificant after controlling for isotopic values of their direct resources, revealing direct bottom-up control and little phylogenetic dependence. By integrating ecosystem and mechanistic perspectives, we found that nutrient dynamics in food webs are governed at the base by the complex interaction between local determinants and evolutionary factors.

The evolutionary convergence of avian lifestyles and their constrained coevolution with species' ecological niche.

The fit between life histories and ecological niche is a paradigm of phenotypic evolution, also widely used to explain patterns of species co-occurrence. By analysing the lifestyles of a sympatric avian assemblage, we show that species' solutions to environmental problems are not unbound. We identify a life-history continuum structured on the cost of reproduction along a temperature gradient, as well as habitat-driven parental behaviour. However, environmental fit and trait convergence are limited by niche filling and by within-species variability of niche traits, which is greater than variability of life histories. Phylogeny, allometry and trade-offs are other important constraints: lifetime reproductive investment is tightly bound to body size, and the optimal allocation to reproduction for a given size is not established by niche characteristics but by trade-offs with survival. Life histories thus keep pace with habitat and climate, but under the limitations imposed by metabolism, trade-offs among traits and species' realized niche.

From inter-specific behavioural interactions to species distribution patterns along gradients of habitat heterogeneity.

The strength of the behavioural processes associated with competitor coexistence may vary when different physical environments, and their biotic communities, come into contact, although empirical evidence of how interference varies across gradients of environmental complexity is still scarce in vertebrates. Here, I analyse how behavioural interactions and habitat selection regulate the local distribution of steppeland larks (Alaudidae) in a gradient from simple to heterogeneous agricultural landscapes in Spain, using crested lark Galerida cristata and Thekla lark G. theklae as study models. Galerida larks significantly partitioned by habitat but frequently co-occurred in heterogeneous environments. Irrespective of habitat divergence, however, the local densities of the two larks were negatively correlated, and the mechanisms beyond this pattern were investigated by means of playback experiments. When simulating the intrusion of the congener by broadcasting the species territorial calls, both larks responded with an aggressive response as intense with respect to warning and approach behaviour as when responding to the intrusion of a conspecific. However, birds promptly responded to playbacks only when congener territories were nearby, a phenomenon that points to learning as the mechanisms through which individuals finely tune their aggressive responses to the local competition levels. Heterospecifics occurred in closer proximity in diverse agro-ecosystems, possibly because of more abundant or diverse resources, and here engage in antagonistic interactions. The drop of species diversity associated with agricultural homogenisation is therefore likely to also bring about the disappearance of the behavioural repertoires associated with species interactions.

Interspecific interactions drive cultural co-evolution and acoustic convergence in syntopic species.

1. Antagonistic interactions have been favourite subjects of studies on species co-evolution, because coexistence among competing species often results in quantifiable character displacement. A common output for competitive interactions is trait divergence, although the opposite phenomenon, convergence, has been proposed to evolve in some instances, for example in the communication behaviour of species that maintain mutually exclusive territories. 2. I use here experimental and observational evidence to study how species interactions drive heterospecific signal convergence and analyse how convergence feeds back to the interaction itself, in the form of aggressive behaviour. I recorded the learned territorial signals of two non-hybridizing larks, Galerida cristata and G. theklae, and used allopatric populations as controls for evaluating acoustic convergence in syntopy. Acoustic variation was analysed with respect to social conditions controlling for other potential agents of natural selection, habitat and climate. 3. Interspecific convergence of Galerida calls peaked in syntopy. Although call acoustic structure was affected by climate and habitat, it matched gradients of density and proximity to congeners even at small local scales. The process of cultural transmission, in which individuals may acquire components of behaviour by copying neighbours, enhances the correlation between call acoustics and the local social milieu. 4. Territories were defended against both species, but playback stimuli of convergent congener calls elicited a stronger aggressive reaction than congener calls from allopatric locations. 5. This study shows that learned behaviours may co-evolve as a consequence of antagonistic interactions, determining reciprocal cultural evolution or cultural co-evolution. As for (biological) co-evolution, the distribution of competing species influences whether a particular area becomes a syntopic environment in which convergence is occurring, or an allopatric environment lacking interactions and reciprocal change. Because of their plastic nature, cultural coadaptations may rapidly shift in response to fluctuating social selection, thus propelling dynamic interactions and fine adjustments to the local environment.

Mimicry as a novel pathway linking biodiversity functions and individual behavioural performances.

The feedback of biodiversity on individual trait variation is a poorly explored mechanistic pathway in ecological research. We analysed the relationship between biodiversity and individual performance by focusing on vocal mimicry, a widespread interaction that may serve in intra- and interspecific communication. We studied the songs of two lark species (genus Galerida) that increase the complexity of their song displays by mimicking other birds, and analysed the influence of bird species richness on individual song performance. The diversity of mimicked species and the prevalence of mimicry increased in areas characterized by great α and γ diversity (i.e. where larks experience more diverse encounters with community members, many of them being highly vocal owing to breeding). Conversely, the variability in species-specific song components peaked where larks were abundant, probably matching the complexity of conspecific social milieu. Some trade-offs existed between homo- and heterospecific complexity, suggesting that larks could change from population- to community-driven song variation by tracking the composition of the auditory environment. Mimicry, which serves communication with conspecifics or predators, may mediate interactions, ultimately cascading to aspects of ecological diversity other than those promoting its complexity.

Predation of experimental nests is linked to local population dynamics in a fragmented bird population.

Artificial nest experiments (ANEs) are widely used to obtain proxies of natural nest predation for testing a variety of hypotheses, from those dealing with variation in life-history strategies to those assessing the effects of habitat fragmentation on the persistence of bird populations. However, their applicability to real-world scenarios has been criticized owing to the many potential biases in comparing predation rates of artificial and natural nests. Here, we aimed to test the validity of estimates of ANEs using a novel approach. We related predation rates on artificial nests to population viability analyses in a songbird metapopulation as a way of predicting the real impact of predation events on the local populations studied. Predation intensity on artificial nests was negatively related to the species' annual population growth rate in small local populations, whereas the viability of large local populations did not seem to be influenced, even by high nest predation rates. The potential of extrapolation from ANEs to real-world scenarios is discussed, as these results suggest that artificial nest predation estimates may predict demographic processes in small structured populations.

Selection for functional performance in the evolution of cuticle hardening mechanisms in insects.

Calcified tissues have repeatedly evolved in many animal lineages and show a tremendous diversity of forms and functions. The cuticle of many insects is enriched with elements other than Calcium, a strategy of hardening that is taxonomically widespread but apparently poorly variable among clades. Here, we investigate the evolutionary potential of the enrichment with metals in insect cuticle at different biological levels. We combined experimental evidence of Zinc content variation in the mandibles of a target species (Chorthippus cazurroi [Bolívar]) with phylogenetic comparative analyses among grasshopper species. We found that mandibular Zinc content was repeatable among related individuals and was associated with an indicator of fitness, so there was potential for adaptive variation. Among species, Zinc enrichment evolved as a consequence of environmental and dietary influences on the physical function of the jaw (cutting and chewing), suggesting a role of natural selection in environmental fit. However, there were also important within and transgenerational environmental sources of similarity among individuals. These environmental influences, along with the tight relationship with biomechanics, may limit the potential for diversification of this hardening mechanism. This work provides novel insights into the diversification of biological structures and the link between evolutionary capacity and intra- and interspecific variation.

Phylogenetic classification of ten novel species belonging to the genus Bifidobacterium comprising B. phasiani sp. nov., B. pongonis sp. nov., B. saguinibicoloris sp. nov., B. colobi sp. nov., B. simiiventris sp. nov., B. santillanense sp. nov., B. miconis sp. nov., B. amazonense sp. nov., B. pluvialisilvae sp. nov., and B. miconisargentati sp. nov.

Ten Bifidobacterium strains, i.e., 6T3, 64T4, 79T10, 80T4, 81T8, 82T1, 82T10, 82T18, 82T24, and 82T25, were isolated from mantled guereza (Colobus guereza), Sumatran orangutan (Pongo abeli), silvery marmoset (Mico argentatus), golden lion tamarin (Leontopithecus rosalia), pied tamarin (Saguinus bicolor), and common pheasant (Phaisanus colchinus). Cells are Gram-positive, non-motile, non-sporulating, facultative anaerobic, and fructose 6-phosphate phosphoketolase-positive. Phylogenetic analyses based on the core genome sequences revealed that isolated strains exhibit close phylogenetic relatedness with Bifidobacterium genus members belonging to the Bifidobacterium bifidum, Bifidobacterium longum, Bifidobacterium pullorum, and Bifidobacterium tissieri phylogenetic groups. Phenotypic characterization and genotyping based on the genome sequences clearly show that these strains are distinct from each of the type strains of the so far recognized Bifidobacterium species. Thus, B. phasiani sp. nov. (6T3 = LMG 32224T = DSM 112544T), B. pongonis sp. nov. (64T4 = LMG 32281T = DSM 112547T), B. saguinibicoloris sp. nov. (79T10 = LMG 32232T = DSM 112543T), B. colobi sp. nov. (80T4 = LMG 32225T = DSM 112552T), B. simiiventris sp. nov. (81T8 = LMG 32226T = DSM 112549T), B. santillanense sp. nov. (82T1 = LMG 32284T = DSM 112550T), B. miconis sp. nov. (82T10 = LMG 32282T = DSM 112551T), B. amazonense sp. nov. (82T18 = LMG 32297T = DSM 112548T), pluvialisilvae sp. nov. (82T24 = LMG 32229T = DSM 112545T), and B. miconisargentati sp. nov. (82T25 = LMG 32283T = DSM 112546T) are proposed as novel Bifidobacterium species.

Evolutionary conservation of within-family biodiversity patterns.

The tendency for species to retain their ancestral biological properties has been widely demonstrated, but the effect of phylogenetic constraints when progressing from species to ensemble-level properties requires further assessment. Here we test whether community-level patterns (environmental shifts in local species richness and turnover) are phylogenetically conserved, assessing whether their similarity across different families of lichens, insects, and birds is dictated by the relatedness of these families. We show a significant phylogenetic signal in the shape of the species richness-elevation curve and the decay of community similarity with elevation: closely related families share community patterns within the three major taxa. Phylogenetic influences are partly explained by similarities among families in conserved traits defining body plan and interactions, implying a scaling of phylogenetic effects from the organismal to the community level. Consequently, the phylogenetic signal in community-level patterns informs about how the historical legacy of a taxon and shared responses among related taxa to similar environments contribute to community assembly and diversity patterns.

Gradual Distance Dispersal Shapes the Genetic Structure in an Alpine Grasshopper.

The location of the high mountains of southern Europe has been crucial in the phylogeography of most European species, but how extrinsic (topography of sky islands) and intrinsic features (dispersal dynamics) have interacted to shape the genetic structure in alpine restricted species is still poorly known. Here we investigated the mechanisms explaining the colonisation of Cantabrian sky islands in an endemic flightless grasshopper. We scrutinised the maternal genetic variability and haplotype structure, and we evaluated the fitting of two migration models to understand the extant genetic structure in these populations: Long-distance dispersal (LDD) and gradual distance dispersal (GDD). We found that GDD fits the real data better than the LDD model, with an onset of the expansion matching postglacial expansions after the retreat of the ice sheets. Our findings suggest a scenario with small carrying capacity, migration rates, and population growth rates, being compatible with a slow dispersal process. The gradual expansion process along the Cantabrian sky islands found here seems to be conditioned by the suitability of habitats and the presence of alpine corridors. Our findings shed light on our understanding about how organisms which have adapted to live in alpine habitats with limited dispersal abilities have faced new and suitable environmental conditions.

Characterizing the spatial structure of songbird cultures.

Recent advances have shown that human-driven habitat transformations can affect the cultural attributes of animal populations in addition to their genetic integrity and dynamics. Here I propose using the song of oscine birds for identifying the cultural spatial structure of bird populations and highlighting critical thresholds associated with habitat fragmentation. I studied song variation over a wide geographical scale in a small and endangered passerine, the Dupont's Lark Chersophilus duponti, focusing on (1) cultural population structure, to determine a statistical representation of spatial variation in song and identify cultural units, and (2) the minimum patch size needed for an individual to develop a stable repertoire. I found that overall song diversity depends on variation among populations (beta-cultural diversity). Abrupt thresholds occurred in the relationships between individual song dissimilarity and geographic distance, and between individual song diversity and patch area. Spatial autocorrelation analysis showed that populations located as little as 5 km apart may have independently evolved their song traditions. Song diversity stabilized in patches as small as 100 ha supporting as few as 8-20 males. Song repertoires of smaller patches were significantly poorer. Almost one-quarter of the study populations inhabited patches <100 ha, and their cultural traditions appear to have eroded. The analysis of spatial patterns in birdsong may be a useful tool for detecting subpopulations prone to extinction.

Phenotypic similarity in sympatric crow species: Evidence of social convergence?

Crows, rooks, and ravens (Corvus spp.) display marked morphological and voice similarities that have been hypothesized to stem from competitive interactions, as a case of nonaposematic mimicry. Here, I test predictions of the mimicry hypothesis at the macrovolutionary scale, examining whether species morphological and acoustic traits covary with those of coexisting congeners, and whether phenotypic similarity has facilitated the coexistence of related species after secondary contact. Body size and the temporal patterns of the commonest call display high levels of similarity among sympatric species, even after controlling for the effect of shared climate and habitat, and phylogenetic constraints in the production of variation. When sister species differed in these acoustic and morphological traits, their transition to secondary sympatry was delayed relative to those with more similar traits. No similarity was found in the sexual call of crows, suggesting that convergence occurs only when function does not favour maintenance of species-specific traits. Crow similarities in morphological and acoustic features may therefore be associated with coevolving interactions with congeners, in line with a broad array of studies documenting convergence among species that interact aggressively or forage communally.

Species partitioning in a temperate mountain chain: Segregation by habitat vs. interspecific competition.

Disentangling the relative influence of the environment and biotic interactions in determining species coexistence patterns is a major challenge in ecology. The zonation occurring along elevation gradients, or at bioclimatic contact zones, offers a good opportunity to improve such understanding because the small scale at which the partitioning occurs facilitates inference based on experiments and ecological modelling. We studied the influence of abiotic gradients, habitat types, and interspecific competition in determining the spatial turnover between two pipit and two bunting species in NW Spain. We explored two independent lines of evidence to draw inference about the relative importance of environment and biotic interactions in driving range partitioning along elevation, latitude, and longitude. We combined occurrence data with environmental data to develop joint species distribution models (JSDM), in order to attribute co-occurrence (or exclusion) to shared (or divergent) environmental responses and to interactions (attraction or exclusion). In the same region, we tested for interference competition by means of playback experiments in the contact zone. The JSDMs highlighted different responses for the two species pairs, although we did not find direct evidence of interspecific aggressiveness in our playback experiments. In pipits, partitioning was explained by divergent climate and habitat requirements and also by the negative correlations between species not explained by the environment. This significant residual correlation may reflect forms of competition others than direct interference, although we could not completely exclude the influence of unmeasured environmental predictors. When bunting species co-occurred, it was because of shared habitat preferences, and a possible limitation to dispersal might cause their partitioning. Our results indicate that no single mechanism dominates in driving the distribution of our study species, but rather distributions are determined by the combination of many small forces including biotic and abiotic determinants of niche, whose relative strengths varied among species.

Landscape bioacoustics allow detection of the effects of habitat patchiness on population structure.

Landscape structure may affect individual dispersal abilities, thus influencing the genotypic and phenotypic composition of populations. We analyzed the interplay among landscape, behavior, and evolutionary processes by correlating habitat patchiness to the variability in vocalizations of Dupont's Lark Chersophilus duponti, one of the most habitat-selective and rare European songbirds. We tape-recorded males throughout the species distribution in Spain, analyzed the spatial patterns of territorial call variation at different scales (individuals, populations, and broad geographic areas), and related acoustic variability to patterns of isolation by geographic distance and by landscape unsuitability (calculated by building a predictive model of habitat suitability). The differentiation of spectro-temporal call features resulted from both isolation by distance and isolation by landscape unsuitability mechanisms. Landscape connectivity was often a better determinant of call differentiation than simple straight-line distance between individuals, providing the first evidence that call transmission can be limited by the presence and distribution of patches of adequate habitat, which likely mediates bird dispersal. Landscape patchiness resulted in a reduction of acoustic diversity (repertoire size) within populations, and a parallel increase in differentiation among populations. Landscape bioacoustics can represent a promising tool for estimating population structure, although the study of animal communication cannot be viewed as an alternative, but a source of complementary information to genetics, given that it provides evidence of male-male transmission and social and cultural phenomena that are currently undetectable from molecular data.

Distress calls may honestly signal bird quality to predators.

In predator-prey interactions, both interactors may benefit from sharing information about prey vulnerability. We examined the relationship between calls used to discourage close predators (distress calls) and the health condition of the caller to test whether these signals are reliable indicators of prey quality. The structure of calls from captured lesser short-toed larks Calandrella rufescens was related to their body condition and T-cell-mediated immunocompetence. Birds in better nutritional and immunological condition utter harsher calls (i.e. they spread the call energy over a wider range of frequency) than birds in poorer conditions. Hence, the harshness of distress calls seems honestly to signal the health status of prey and thus their ability to escape, on which the predator might base its optimal foraging choice. Previous studies have investigated the honesty of songs that have evolved via sexual selection, but this is the first study, to our knowledge, the demonstrates a relationship between individual quality and a vocalization primarily shaped by natural selection.

Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems.

In social insects, cuticular hydrocarbons (CHCs) play an important role in nestmate discrimination processes, but young individuals are usually not discriminated. We studied CHC changes in young workers of the social wasp Polistes dominulus. A quantitative estimation demonstrated that total quantities of CHCs increased after emergence, with branched alkanes increasing drastically when compared with other classes of hydrocarbons. The relative quantity of longer-chain compounds increased with respect to shorter ones; unsaturated compounds decreased. These changes might reduce the capacity of the cuticle to acquire compounds of environmental origin. We then tested whether individuals acquire hydrocarbons from the environment, and whether this capability equally characterises newly emerged and mature wasps. We exposed wasps of two age classes (adults younger or older than 24 h) to four linear hydrocarbons in turn, and observed how nestmates reacted to their re-introduction into the natal colony. Exposed young wasps elicited significantly more aggressive responses than control sisters; but treated wasps older than 24 h were generally accepted by nestmates. Chemical assays showed that exposed young wasps readily absorbed hydrocarbons; older ones did not incorporate hydrocarbons, suggesting that the chemical profiles of mature wasps are less prone to chemical shifts than those of newly emerged wasps.

Climate-driven variation in the intensity of a host-symbiont animal interaction along a broad elevation gradient.

Gradients of environmental stress may affect biotic interactions in unpredictable ways responding to climate variation, depending on the abiotic stress tolerance of interacting partners. Here, we study the effect of local climate on the intensity of feather mites in six mountain passerines along a 1400 m elevational gradient characterized by shifting temperature and rainfall. Although obligatory symbionts of warm-blooded organisms are assumed to live in mild and homeothermic environments, those inhabiting external, non-blood-irrigated body portions of the host organism, such as feather mites, are expected to endure exposure to the direct influence of a fluctuating climate. As expected, feather mite intensity declined with elevation in all bird species, a pattern that was also found in cold-adapted passerines that have typical alpine habits. The elevation cline was mainly explained by a positive effect of the average temperature upon mite intensity in five of the six species studied. Precipitation explained less variance in mite intensity than average temperature, and showed a negative correlation in half of the studied species. We found no climate-driven migration of mites along the wings of birds, no replacement of mite species along elevation gradients and no association with available food resources for mites (estimated by the size of the uropygial gland). This study suggests that ectosymbionts of warm-blooded animals may be highly sensitive to climatic variation and become less abundant under stressful environmental conditions, providing empirical evidence of the decline of specialized biotic interactions among animal species at high elevations.