Phylogeny and historical biogeography of the swallow family (Hirundinidae) inferred from comparisons of thousands of UCE loci.

Swallows (Hirundinidae) are a globally distributed family of passerine birds that exhibit remarkable similarity in body shape but tremendous variation in plumage, sociality, nesting behavior, and migratory strategies. As a result, swallow species have become models for empirical behavioral ecology and evolutionary studies, and variation across the Hirundinidae presents an excellent opportunity for comparative analyses of trait evolution. Exploiting this potential requires a comprehensive and well-resolved phylogenetic tree of the family. To address this need, we estimated swallow phylogeny using genetic data from thousands of ultraconserved element (UCE) loci sampled from nearly all recognized swallow species. Maximum likelihood, coalescent-based, and Bayesian approaches yielded a well-resolved phylogenetic tree to the generic level, with minor disagreement among inferences at the species level, which likely reflect ongoing population genetic processes. The UCE data were particularly useful in helping to resolve deep nodes, which previously confounded phylogenetic reconstruction efforts. Divergence time estimates from the improved swallow tree support a Miocene origin of the family, roughly 13 million years ago, with subsequent diversification of major groups in the late Miocene and Pliocene. Our estimates of historical biogeography support the hypothesis that swallows originated in the Afrotropics and have subsequently expanded across the globe, with major in situ diversification in Africa and a secondary major radiation following colonization of the Neotropics. Initial examination of nesting and sociality indicates that the origin of mud nesting - a relatively rare nest construction phenotype in birds - was a major innovation coincident with the origin of a clade giving rise to over 40% of extant swallow diversity. In contrast, transitions between social and solitary nesting appear less important for explaining patterns of diversification among swallows.

Passerine sister clade comparisons reveal variable macroevolutionary outcomes of interhemispheric dispersal.

Dispersal events offer a unique window into macroevolutionary processes, especially with respect to the effects of competition on diversification. Empirical studies testing alternative predictions of competitive effects are often limited in either geographic or phylogenetic scale. Here, we tested some of these hypotheses by comparing an assemblage of 16 oscine passerine clades, representing independent dispersal events into the Western Hemisphere, to their sister clades in the Eastern Hemisphere. We also compared the diversity of this assemblage of clades to an older, incumbent passerine clade in the Western Hemisphere, the suboscines. Specifically, we tested for ecological opportunity and incumbency-mediated constraints by analysis of clade-specific morphological disparities and rates of evolution relative to dispersal history. While there was no consistent outcome of oscine dispersal and macroevolution in the Western Hemisphere relative to their Eastern Hemisphere sister groups, most clades supported a role for ecological opportunity or incumbency effects, and such effects were better explained by differences in species accumulation than by differences in rates of trait evolution or colonization timing. This general pattern was not evident when comparing the entire oscine assemblage of the Western Hemisphere to the incumbent suboscine radiation; oscines and suboscines occupy comparable regions of functional trait diversity and, despite higher rates of trait evolution in oscines, these observations were consistent with simulated null expectations. This result suggests that oscine and suboscine assemblages may have evolved in relative isolation for a significant fraction of their history.

Chasing and surfing seasonal waves: Avian migration through the US tracks land surface phenology in fall, but not spring.

Climate change is altering the timing of seasonal events for many taxa. There is limited understanding of how northward/southward songbird migration follows or is limited by the latitudinal progression of seasonal transitions. Consistent environmental conditions that migrating birds encounter across latitudes likely represent or correlate with important resources or limiting factors for migration. We tested whether migratory passage-observed via radar-consistently tracked land surface variables and phenophases across latitudes in the US Central Flyway in both spring and fall. The daily temperatures, precipitation and vegetation greenness occurring on 10%, 50% and 90% cumulative passage dates changed substantially with latitude, indicating that most migrants experienced rapidly changing conditions as they headed north or south. Temperature did not limit the progression of migration in either season. Peak spring migration in the southern US occurred nearly 40 days after the spring green wave, the northward progression of vegetation growth, but nearly caught up to green-up at 48° N. Spring migration phenology may have evolved to prioritize earlier arrival for breeding. Across all latitudes, peak fall migration coincided with the same land surface phenophase, an interval of 26 days prior to dormancy onset. Migrants may rely on phenological events in vegetation during fall stopovers. Considering that (a) migratory passage tracked fall land surface phenology across latitudes at a continental scale, (b) previous studies at local scales have demonstrated the importance of fruit during fall migratory stopover and (c) fruiting phenology in North America is occurring later over time while fall migration is advancing, the potential for mismatch between fall fruiting and bird migration phenology urgently needs further investigation.

Comparative anatomy of the passerine carpometacarpus helps illuminate the early fossil record of crown Passeriformes.

The hyper-diverse clade Passeriformes (crown group passerines) comprises over half of extant bird diversity, yet disproportionately few studies have targeted passerine comparative anatomy on a broad phylogenetic scale. This general lack of research attention hinders efforts to interpret the passerine fossil record and obscures patterns of morphological evolution across one of the most diverse clades of extant vertebrates. Numerous potentially important crown passeriform fossils have proven challenging to place phylogenetically, due in part to a paucity of phylogenetically informative characters from across the passerine skeleton. Here, we present a detailed analysis of the morphology of extant passerine carpometacarpi, which are relatively abundant components of the passerine fossil record. We sampled >70% of extant family-level passerine clades (132 extant species) as well as several fossils from the Oligocene of Europe and scored them for 54 phylogenetically informative carpometacarpus characters optimised on a recently published phylogenomic scaffold. We document a considerable amount of previously undescribed morphological variation among passerine carpometacarpi, and, despite high levels of homoplasy, our results support the presence of representatives of both crown Passeri and crown Tyranni in Europe during the Oligocene.

Biocompatible polymeric microparticles serve as novel and reliable vehicles for exogenous hormone manipulations in passerines.

The administration of exogenous hormones emerged as an essential tool for field studies in endocrinology. However, working with wild animals remains challenging, because under field conditions not every available method meets the necessary requirements. Achieving a sustained elevation in hormone levels, while simultaneously minimising handling time and invasiveness of the procedure is a difficult task in field endocrinology. Facing this challenge, we have investigated the suitability of biocompatible polymeric microparticles, a novel method for drug-administration, as a tool to manipulate hormones in small songbirds. We chose the insulin-like growth factor-1 (IGF-1) as target hormone, because it receives great interest from the research community due to its important role in shaping life-history traits. Moreover, its short half-life and hydrophilic properties imply a major challenge in finding a suitable method to achieve a sustained, systemic long-term release. To study the release kinetics, we injected either IGF-1 loaded polylactic-co-glycolic acid (PLGA) microparticles or dispersion medium (control group) in the skin pocket of the interscapular region of captive bearded reedlings (Panurus biarmicus). We collected blood samples for 7 consecutive days plus an additional sampling period after two weeks and complemented these with an in vitro experiment. Our results show that in vitro, PLGA microparticles allowed a stable IGF-1 release for more than 15 days, following a burst release at the beginning of the measurement. In vivo, the initial burst was followed by a drop to still elevated levels in circulating IGF-1 until the effect vanished by 16 days post-treatment. This study is the first to describe the use of PLGA-microparticles as a novel tool for exogenous hormone administration in a small passerine. We suggest that this method is highly suitable to achieve the systemic long-term release of hydrophilic hormones with short half-life and reduces overall handling time, as it requires only one subcutaneous injection.

Competition and hybridization drive interspecific territoriality in birds.

Costly interactions between species that arise as a by-product of ancestral similarities in communication signals are expected to persist only under specific evolutionary circumstances. Territorial aggression between species, for instance, is widely assumed to persist only when extrinsic barriers prevent niche divergence or selection in sympatry is too weak to overcome gene flow from allopatry. However, recent theoretical and comparative studies have challenged this view. Here we present a large-scale, phylogenetic analysis of the distribution and determinants of interspecific territoriality. We find that interspecific territoriality is widespread in birds and strongly associated with hybridization and resource overlap during the breeding season. Contrary to the view that territoriality only persists between species that rarely breed in the same areas or where niche divergence is constrained by habitat structure, we find that interspecific territoriality is positively associated with breeding habitat overlap and unrelated to habitat structure. Furthermore, our results provide compelling evidence that ancestral similarities in territorial signals are maintained and reinforced by selection when interspecific territoriality is adaptive. The territorial signals linked to interspecific territoriality in birds depend on the evolutionary age of interacting species, plumage at shallow (within-family) timescales, and song at deeper (between-family) timescales. Evidently, territorial interactions between species have persisted and shaped phenotypic diversity on a macroevolutionary timescale.

Mediterranean songbirds show pronounced seasonal variation in thermoregulatory traits.

Addressing the patterns of variation in thermal traits is crucial to better predict the potential effects of climate change on organisms. Here, we assessed seasonal (winter vs summer) adjustments in key thermoregulatory traits in eight Mediterranean-resident songbirds. Overall, songbirds increased whole-animal (by 8%) and mass-adjusted (by 9%) basal metabolic rate and decreased (by 56%) thermal conductance below the thermoneutral zone during winter. The magnitude of these changes was within the lower values found in songbirds from northern temperate areas. Moreover, songbirds increased (by 11%) evaporative water loss within the thermoneutral zone during summer, while its rate of increase above the inflection point of evaporative water loss (i.e., the slope of evaporative water loss versus temperature) decreased by 35% during summer - a value well above that reported for other temperate and tropical songbirds. Finally, body mass increased by 5% during winter, a pattern similar to that found in many northern temperate species. Our findings support the idea that physiological adjustments might enhance the resilience of Mediterranean songbirds to environmental changes, with short-term benefits by saving energy and water under thermally stressful conditions. Nevertheless, not all species showed the same patterns, suggesting different strategies in their thermoregulatory adaptations to seasonal environments.

Verification of accuracy of qPCR method for intravital diagnostics of Macrorhabdus ornithogaster in avian droppings.

The objective of this study was to verify the accuracy of the quantitative PCR (qPCR) method for in vivo detection of Macrorhabdus ornithogaster. A total of 100 faecal and gastric mucosa samples from avian cadavers were investigated, using cytological and qPCR techniques (budgerigars, Fischer's lovebirds, red-crowned parakeets, scarlet-chested parrots, eastern rosellas, domestic canaries, zebra finches, white Java sparrow). Using qPCR, the probability of detecting positive samples of droppings was significantly higher than in the faecal smear microscopy (P < 0.01). Cytology detected the presence of Macrorhabdus ornithogaster in 34 faecal samples, whereas qPCR detected 54 positive samples. In all 46 qPCR negative faecal samples, gastric smear qPCR was performed and also yielded negative results. Gastric smear qPCR was also performed in 20 cadavers where faecal qPCR has detected the presence of Macrorhabdus ornithogaster and in all samples confirmed the positive result. This verifies the accuracy of faecal sample qPCR for intravital diagnostics. Overall, the faecal qPCR technique appears to be extremely reliable, as it made it possible to detect all infected individuals, including those with negative stool or gastric cytology.

Cryptic species in a colorful genus: Integrative taxonomy of the bush robins (Aves, Muscicapidae, Tarsiger) suggests two overlooked species.

Several cryptic avian species have been validated by recent integrative taxonomic efforts in the Sino-Himalayan mountains, indicating that avian diversity in this global biodiversity hotspot may be underestimated. In the present study, we investigated species limits in the genus Tarsiger, the bush robins, a group of montane forest specialists with high species richness in the Sino-Himalayan region. Based on comprehensive sampling of all 11 subspecies of the six currently recognized species, we applied an integrative taxonomic approach by combining multilocus, acoustic, plumage and morphometric analyses. Our results reveal that the isolated north-central Chinese populations of Tarsiger cyanurus, described as the subspecies albocoeruleus but usually considered invalid, is distinctive in genetics and vocalisation, but only marginally differentiated in morphology. We also found the Taiwan endemic T. indicus formosanus to be distinctive in genetics, song and morphology from T. i. indicus and T. i. yunnanensis of the Sino-Himalayan mountains. Moreover, Bayesian species delimitation using BPP suggests that both albocoeruleus and formosanus merit full species status. We propose their treatment as 'Qilian Bluetail' T. albocoeruleus and 'Taiwan Bush Robin' T. formosanus, respectively.

Evolutionary trade-off between male colouration and feather moult extent also indirectly determines female moult.

Males and females are often influenced by different selective forces, frequently resulting in diverging phenotypes, for example in colouration. Since an animal's colouration may strongly influence its fitness, causes and consequences of sexual dichromatism in birds could aid in understanding important factors affecting sexual and natural selection. Variation in plumage ornamentation may affect mate attraction or intraspecific antagonistic behaviour. In most passerines, body plumage colouration of juveniles is obtained through the process of feather moult. The number of moulted wing and tail feathers, which also influences the bird's appearance, may affect its fitness. Here, we show that body plumage colouration of male, but not female, passerines is correlated with the number of moulted wing and tail feathers in the early stage of the bird's life for both sexes. Thus, the extent of wing and tail moult in females is not modulated by the female's colouration and can prevent females from reaching their sex-specific optima. This result could be explained by high intersexual genetic correlations, which might make it impossible for the sexes to reach their own trait fitness optima. Our findings may indicate that species-specific, rather than sex-specific, internal correlations shaped bird moult strategy, an important avian life-history trait.

Heat tolerance limits of Mediterranean songbirds and their current and future vulnerabilities to temperature extremes.

Songbirds are one of the groups most vulnerable to extreme heat events. Although several recent studies have assessed their physiological responses to heat, most of them have focused solely on arid-zone species. We investigated thermoregulatory responses to heat in eight small-sized songbirds occurring in the Mediterranean Basin, where heatwaves are becoming more frequent and intense. Specifically, we determined their heat tolerance limits (HTLs) and evaporative cooling efficiency, and evaluated their current and future vulnerabilities to heat in southwestern Iberia, a Mediterranean climate warming hotspot. To do this, we exposed birds to an increasing profile of air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), evaporative cooling efficiency (the ratio between evaporative heat loss and metabolic heat production) and body temperature (Tb). HTL ranged between 40 and 46°C across species, and all species showed rapid increases in RMR, EWL and Tb in response to increasing Ta. However, only the crested lark (Galerida cristata) achieved an evaporative cooling efficiency greater than 1. The studied songbirds currently experience summer Ta maxima that surpass the upper critical temperatures of their thermoneutral zone and even their HTL. Our estimates indicate that five of the eight species will experience moderate risk of lethal dehydration by the end of the century. We argue that the limited heat tolerance and evaporative cooling efficiency of small-sized Mediterranean songbirds make them particularly vulnerable to heatwaves, which will be exacerbated under future climate change scenarios.

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.

Multiple trace elements exposure of Grey-cheeked Fulvettas Alcippe morrisonia, a nuclear member in bird mixed-species flocks, and implications for bioindicator.

Birds are vulnerable to metal pollution, which can serve as indicators of environmental safety monitoring. In this study, we evaluated three non-essential (Pb, Cd, and As) and two essential (Cu and Zn) trace elements of living (only feathers) and deceased (feathers and tissues) Grey-cheeked Fulvetta (Alcippe morrisonia) at a highly polluted mine tailings and a reference site. Five metal concentrations in the feathers of living Grey-cheeked Fulvettas were higher at the mine site. Among these, the levels of Cd and Pb in most feathers exceeded the threshold, resulting in an ecotoxicological concern. The correlation analysis suggested that feathers from Grey-cheeked Fulvettas might be useful bioindicators for local metal contamination assessment. The toxicological effects of trace metals on Grey-cheeked Fulvetta might affect its leadership ability. Therefore, understanding the effects of metal pollution on Grey-cheeked Fulvetta would show important practical implications for the conservation of bird communities.

Isotope record tracks changes in historical wintering ranges of a passerine in sub-Saharan Africa.

Billions of birds migrate from the Palaearctic to sub-Saharan Africa, yet we are unaware about where exactly they stay over winter and how consistent they have been using these wintering areas over historical times. Here, we inferred the historical wintering areas of Eurasian Golden Orioles (Oriolus oriolus) from stable isotope ratios of feathers. Over the past 200 years, Golden Orioles used two major wintering grounds. Between 1895 and 1971, the relative use of these areas depended on local rainfall intensities. Golden Orioles may depend strongly on humid wintering areas in sub-Saharan Africa, which may put this species at stake when the global climate continues to change.

A test of altitude-related variation in aerobic metabolism of Andean birds.

Endotherms at high altitude face the combined challenges of cold and hypoxia. Cold increases thermoregulatory costs, and hypoxia may limit both thermogenesis and aerobic exercise capacity. Consequently, in comparisons between closely related highland and lowland taxa, we might expect to observe consistent differences in basal metabolic rate (BMR), maximal metabolic rate (MMR) and aerobic scope. Broad-scale comparative studies of birds reveal no association between BMR and native elevation, and altitude effects on MMR have not been investigated. We tested for altitude-related variation in aerobic metabolism in 10 Andean passerines representing five pairs of closely related species with contrasting elevational ranges. Mass-corrected BMR and MMR were significantly higher in most highland species relative to their lowland counterparts, but there was no uniform elevational trend across all pairs of species. Our results suggest that there is no simple explanation regarding the ecological and physiological causes of elevational variation in aerobic metabolism.

Climate and weather have differential effects in a high latitude passerine community.

Climatic factors act on populations at multiple timescales leading to the separation of long-term climate and shorter-term weather effects. We used passerine counts from 1995 to 2019 in subarctic Alaska (Denali National Park, USA) to assess the impacts of the prior breeding season's weather on breeding season abundance and the impacts of climate measured through shifts in elevational distribution. Weather and climate appear to have had opposing effects on the abundance of some shrub-associated species as evidenced by a positive response to nesting phase temperature over a 1-year lag and a negative response to warming-induced shifts in shrub-dominated habitats over the long term. The latter response was indicated by declines in abundance which occurred in some part through portions of these populations shifting upslope of our fixed sampling frame. Overall, the abundance of species was related to one or more of the lagged effects of weather and the effects of weather alone drove nearly twofold variation in annual abundance in most species. The effect of nesting phase temperature was a strong positive predictor at both community and individual species levels, whereas arrival phase temperature had weak support at both levels. The effects of total precipitation during the nesting phase and snowmelt timing shared mixed support at community and species levels, but generally indicated higher abundance following seasons that were drier and had earlier snowmelt. Together, our findings of opposing effects of climatic variables at different timescales have implications for understanding the mechanisms of population and distributional change in passerines in the subarctic.

Tick infestation on birds in an urban Atlantic Forest fragment in north-eastern Brazil.

Birds are important hosts for various tick species, playing a significant role in their biological life cycle and dispersion. In this study, we investigated tick infestations on birds trapped in an urban remnant of Atlantic Forest in Pernambuco state, Brazil. From February 2015 to March 2017, 541 birds belonging to 52 species were trapped with mist nets and examined for ectoparasites. Birds trapped in the late successional forest were significantly more infested than birds trapped in the early successional forest. In the same way, ectoparasite infestation varied significantly according to bird weight and collection plot. Overall, 198 birds (36.6%) belonging to 27 species were parasitized by ectoparasites (i.e., ticks, lice and/or mites). Ectoparasites were effectively collected from 111 birds, of which 99 belonging to 20 species were infested by ticks (n = 261), namely, Amblyomma longirostre (13 nymphs), Amblyomma nodosum (21 nymphs), Amblyomma varium (one nymph), and Amblyomma spp. (five nymphs and 221 larvae). Most of the ticks (> 90%) were collected from Passeriformes. This study provides the second record of A. varium in Pernambuco state and confirms that birds, especially Passeriformes, are important hosts for larvae and nymphs of Amblyomma spp. in the Atlantic Forest biome of Pernambuco.

Daily Nest Predation Rates Decrease with Body Size in Passerine Birds.

AbstractBody size evolution is generally framed by the benefits of being large, while costs are largely overlooked. An important putative cost of being large is the need to extend development periods, which should increase exposure to predation and potentially select against larger size. In birds, this selection pressure can be important because predation is the main source of offspring mortality and predators should more readily detect the larger nests associated with larger body sizes. Here, we show for diverse passerine birds across the world that counter to expectations, larger species suffer lower daily nest predation rates than smaller species. This pattern is consistent despite latitudinal variation in predation and does not seem to reflect a tendency of larger species to use more protected nests or less exposed nest locations. Evidence instead suggests that larger species attack a wider array of predator sizes, which could reduce predation rates in nests of large-bodied species. Regardless of the mechanism, the lower daily nest predation rates of larger species yield slightly lower predation rates over the entire development period compared with smaller species. These results highlight the importance of behavior as a mechanism to alter selection pressures and have implications for body size evolution.

Age-dependent phenological plasticity in a wild bird.

Life-history traits are often plastic in response to environmental factors such as temperature or precipitation, and they also vary with age in many species. Trait variation during the lifetime could thus be partly driven by age-dependent plasticity in these traits. We study whether plasticity of a phenological trait-the egg-laying date-with respect to spring temperature, varies with age, and explore whether this variation relates to changes in breeding success throughout the life cycle. We use data from a four-decade long-term monitoring of a wild population of blue tits in Corsica, to estimate age-dependent plasticity of reproductive phenology and annual reproductive success. We show that both laying date plasticity and annual reproductive success vary with age: young and old females are less plastic, and fledge fewer offspring, than middle-age females. Furthermore, in contrast to young and prime-age females, in old females fledging success does not depend on laying date. Phenological plasticity is a major mechanism for coping with rapid environmental variation. Our results suggest that understanding its role in adaptation to climate change and population persistence requires integrating the age structure of the population.

Frequent nocturnal torpor in a free-ranging Australian honeyeater, the noisy miner.

Torpor in birds is considered to be far less common than in mammals. This is particularly true for passerine birds for which knowledge of torpor expression is scarce, although almost all are small, have high energy expenditure and could profit energetically from using torpor. To assess whether the extent and diversity of avian and especially passerine torpor expression and heterothermy may be currently underestimated because of limited long-term data on free-ranging birds, core body temperature fluctuations were quantified over ~ 4.3 months in a medium-sized honeyeater, the noisy miner (Manorina melanocephala, ~ 75 g), in an open woodland during the cold season in eastern Australia. Miners used shallow nocturnal torpor frequently (63% of days), torpor bouts lasted on average for 6.5 h (maximum 13.5 h) and, unlike during hypothermia, torpor was terminated by endogenous heat production for rewarming. Body temperatures (Tb) ranged from a maximum of 43.5 °C to a minimum of 33.0 °C, often fell by 7 °C at night, and the overall mean Tb was 38.7 ± 0.7 °C. The data show that yet another passerine bird, widely viewed to be homeothermic, expresses torpor in the wild for energy conservation. Considering the size of miners, it seems probable that many other, especially smaller birds, use a similar approach at least in winter to enhance the chance of survival in the face of high energy expenditure and low food availability.