Selection on VPS13A linked to migration in a songbird.

Animal migration demands an interconnected suite of adaptations for individuals to navigate over long distances. This trait complex is crucial for small birds whose migratory behaviors-such as directionality-are more likely innate, rather than being learned as in many longer-lived birds. Identifying causal genes has been a central goal of migration ecology, and this endeavor has been furthered by genome-scale comparisons. However, even the most successful studies of migration genetics have achieved low-resolution associations, identifying large chromosomal regions that encompass hundreds of genes, one or more of which might be causal. Here we leverage the genomic similarity among golden-winged (Vermivora chrysoptera) and blue-winged (V. cyanoptera) warblers to identify a single gene-vacuolar protein sorting 13A (VPS13A)-that is associated with distinct differences in migration to Central American (CA) or South American (SA) wintering areas. We find reduced sequence variation in this gene region for SA wintering birds, and show this is the likely result of natural selection on this locus. In humans, variants of VPS13A are linked to the neurodegenerative disorder chorea-acanthocytosis. This association provides one of the strongest gene-level associations with avian migration differences.

Population trends in Vermivora warblers are linked to strong migratory connectivity.

Migratory species can experience limiting factors at different locations and during different periods of their annual cycle. In migratory birds, these factors may even occur in different hemispheres. Therefore, identifying the distribution of populations throughout their annual cycle (i.e., migratory connectivity) can reveal the complex ecological and evolutionary relationships that link species and ecosystems across the globe and illuminate where and how limiting factors influence population trends. A growing body of literature continues to identify species that exhibit weak connectivity wherein individuals from distinct breeding areas co-occur during the nonbreeding period. A detailed account of a broadly distributed species exhibiting strong migratory connectivity in which nonbreeding isolation of populations is associated with differential population trends remains undescribed. Here, we present a range-wide assessment of the nonbreeding distribution and migratory connectivity of two broadly dispersed Nearctic-Neotropical migratory songbirds. We used geolocators to track the movements of 70 Vermivora warblers from sites spanning their breeding distribution in eastern North America and identified links between breeding populations and nonbreeding areas. Unlike blue-winged warblers (Vermivora cyanoptera), breeding populations of golden-winged warblers (Vermivora chrysoptera) exhibited strong migratory connectivity, which was associated with historical trends in breeding populations: stable for populations that winter in Central America and declining for those that winter in northern South America.

A wood-warbler produced through both interspecific and intergeneric hybridization.

Hybridization between divergent taxa can provide insight into the breakdown of characters used in mate choice, as well as reproductive compatibility across deep evolutionary timescales. Hybridization can also occur more frequently in declining populations, as there is a smaller pool of conspecific mates from which to choose. Here, we report an unusual combination of factors that has resulted in a rare, three-species hybridization event among two genera of warblers, one of which is experiencing significant population declines. We use bioacoustic, morphometric and genetic data, to demonstrate that an early generation female hybrid between a golden-winged warbler (Vermivora chrysoptera) and a blue-winged warbler (V. cyanoptera) went on to mate and successfully reproduce with a chestnut-sided warbler (Setophaga pensylvanica). We studied the product of this event-a putative chrysoptera × cyanoptera × pensylvanica hybrid-and show that this male offspring sang songs like S. pensylvanica, but had morphometric traits similar to Vermivora warblers. The hybrid's maternal parent had V. chrysoptera mitochondrial DNA and, with six plumage-associated loci, we predicted the maternal parent's phenotype to show that it was likely an early generation Vermivora hybrid. That this hybridization event occurred within a population of Vermivora warblers in significant decline suggests that females may be making the best of a bad situation, and that wood-warblers in general have remained genetically compatible long after they evolved major phenotypic differences.

Retirement investment theory explains patterns in songbird nest-site choice.

When opposing evolutionary selection pressures act on a behavioural trait, the result is often stabilizing selection for an intermediate optimal phenotype, with deviations from the predicted optimum attributed to tracking a moving target, development of behavioural syndromes or shifts in riskiness over an individual's lifetime. We investigated nest-site choice by female golden-winged warblers, and the selection pressures acting on that choice by two fitness components, nest success and fledgling survival. We observed strong and consistent opposing selection pressures on nest-site choice for maximizing these two fitness components, and an abrupt, within-season switch in the fitness component birds prioritize via nest-site choice, dependent on the time remaining for additional nesting attempts. We found that females consistently deviated from the predicted optimal behaviour when choosing nest sites because they can make multiple attempts at one fitness component, nest success, but only one attempt at the subsequent component, fledgling survival. Our results demonstrate a unique natural strategy for balancing opposing selection pressures to maximize total fitness. This time-dependent switch from high to low risk tolerance in nest-site choice maximizes songbird fitness in the same way a well-timed switch in human investor risk tolerance can maximize one's nest egg at retirement. Our results also provide strong evidence for the adaptive nature of songbird nest-site choice, which we suggest has been elusive primarily due to a lack of consideration for fledgling survival.

Regional variation in immature Ixodes scapularis parasitism on North American songbirds: implications for transmission of the Lyme pathogen, Borrelia burgdorferi.

Borrelia burgdorferi, the etiological agent of Lyme disease, is transmitted among hosts by the black-legged tick, Ixodes scapularis, a species that regularly parasitizes various vertebrate hosts, including birds, in its immature stages. Lyme disease risk in the United States is highest in the Northeast and in the upper Midwest where I. scapularis ticks are most abundant. Because birds might be important to the range expansion of I. scapularis and B. burgdorferi, we explored spatial variation in patterns of I. scapularis parasitism on songbirds, as well as B. burgdorferi infection in bird-derived I. scapularis larvae. We sampled birds at 23 sites in the eastern United States to describe seasonal patterns of I. scapularis occurrence on birds, and we screened a subset of I. scapularis larvae for presence of B. burgdorferi. Timing of immature I. scapularis occurrence on birds is consistent with regional variation in host-seeking activity with a generally earlier peak in larval parasitism on birds in the Midwest. Significantly more I. scapularis larvae occurred on birds that were contemporaneously parasitized by nymphs in the Midwest than the Northeast, and the proportion of birds that yielded B. burgdorferi-infected larvae was also higher in the Midwest. We conclude that regional variation in immature I. scapularis phenology results in different temporal patterns of parasitism on birds, potentially resulting in differential importance of birds to B. burgdorferi transmission dynamics among regions.

Extensive historical and contemporary hybridization suggests premating isolation in Vermivora warblers is not strong: A reply to Confer et al.

We present comments on an article published by Confer et al. (Ecology and Evolution, 10, 2020). Confer et al. (2020) aggregate data from multiple studies of social pairing between Vermivora chrysoptera and V. cyanoptera, two wood warblers in the family Parulidae that hybridize extensively where they co-occur. From analysis of these data, they conclude there is near-complete reproductive isolation between these two species. In our reply, we show that this finding is not supported by other lines of evidence, and significant drawbacks of their study design preclude such strong conclusions. In our critique, we show that (a) coarse-scale plumage classifications cannot be used to accurately estimate hybrid ancestry in Vermivora; (b) extra-pair paternity is very high in Vermivora and is likely facilitating hybridization, yet was not considered by Confer et al. (2020), and we suggest this will have a substantial influence on the interpretation of reproductive isolation in the system; and (c) the central finding of strong total reproductive isolation is not compatible with the results of other long-term studies, which demonstrate low isolation and high gene flow. We conclude with a more comprehensive interpretation of hybridization and reproductive isolation in Vermivora warblers.

Effects of harmful algal blooms on stress levels and immune functioning in wetland-associated songbirds and reptiles.

Harmful algal blooms (HABs), caused primarily by nutrient input from agricultural runoff, are a threat to freshwater systems worldwide, and are further predicted to increase in size, frequency, and intensity due to climate change. HABs occur annually in the Western Basin of Lake Erie (Ohio, USA), and these blooms become toxic when dominated by cyanobacteria that produce the liver toxin microcystin. Although we are making substantial inroads toward understanding how microcystin affects human health, less is known about effects of microcystin on wildlife exposed to HABs. Wetland-associated songbirds (barn swallows, Hirundo rustica, and red-winged blackbirds, Agelaius phoeniceus) and reptiles (Northern watersnakes, Nerodia sipedon, and painted turtles, Chrysemys picta) were sampled from wetlands exposed to chronically high microcystin levels due to a prolonged HAB event, and from unexposed, control wetlands. Physiological stress levels and several measures of immune functioning were compared between the HAB-exposed and control populations. Physiological stress levels, measured as heterophil:lymphocyte ratios, were higher in barn swallows, red-winged blackbirds, and Northern watersnakes exposed to a chronic HAB compared to unexposed, control individuals, but painted turtles did not differ in physiological stress levels between HAB-exposed and control individuals. Neither barn swallows nor red-winged blackbirds differed in immune functioning between populations, but HAB-exposed watersnakes had higher bactericidal capacity than control snakes, and HAB-exposed painted turtles had lower bactericidal capacity than control turtles. These results suggest that even when HABs do not cause direct mortality of exposed wildlife, they can potentially act as a physiological stressor across several taxa, and furthermore may compromise immune functioning in some species.

All tests are imperfect: Accounting for false positives and false negatives using Bayesian statistics.

Tests with binary outcomes (e.g., positive versus negative) to indicate a binary state of nature (e.g., disease agent present versus absent) are common. These tests are rarely perfect: chances of a false positive and a false negative always exist. Imperfect results cannot be directly used to infer the true state of the nature; information about the method's uncertainty (i.e., the two error rates and our knowledge of the subject) must be properly accounted for before an imperfect result can be made informative. We discuss statistical methods for incorporating the uncertain information under two scenarios, based on the purpose of conducting a test: inference about the subject under test and inference about the population represented by test subjects. The results are applicable to almost all tests. The importance of properly interpreting results from imperfect tests is universal, although how to handle the uncertainty is inevitably case-specific. The statistical considerations not only will change the way we interpret test results, but also how we plan and carry out tests that are known to be imperfect. Using a numerical example, we illustrate the post-test steps necessary for making the imperfect test results meaningful.

Life history characteristics of birds influence patterns of tick parasitism.

Introduction: Birds serve as reservoirs for tick-borne pathogens as well as hosts for multiple tick species of public health relevance.  Birds may perpetuate life cycles of vectors and vector-borne pathogens and disperse disease vectors over long distances, supplementing populations at range margins or seeding invading populations beyond the edges of current tick distributions.  Our goal for this study was to identify life history characteristics of birds that most strongly affect tick parasitism. Materials and Methods: We collected 6203 ticks from 5426 birds from two sites in eastern North America and used field-derived parasitism data and published literature to analyze impacts of life history factors on tick parasitism in birds. Results and Discussion: We identified body size and nest site to have the strongest impact on tick prevalence and abundance in the songbird species included in this study.  Our findings reveal site-independent patterns in tick parasitism on birds and suggest that physical more than behavioral characteristics may influence a bird species' suitability as a host for ticks. Conclusions: The data and results published here will contribute to a growing body of literature and information on bird-tick interactions and will help elucidate patterns of tick and tick-borne pathogen geographic expansion.

Correction: Evaluating outcomes of management targeting the recovery of a migratory songbird of conservation concern.

[This corrects the article DOI: 10.7717/peerj.4319.].

Is dietary or microhabitat specialization associated with environmental heterogeneity in horned lizards (Phrynosoma)?

Niche breadth is predicted to correlate with environmental heterogeneity, such that generalists will evolve in heterogeneous environments and specialists will evolve in environments that vary less over space and time. We tested the hypothesis that lizards in a heterogeneous environment were generalists compared to lizards in a homogeneous environment. We compared niche breadths of greater short-horned lizards by quantifying resource selection in terms of two different niche axes, diet (prey items and trophic level), and microhabitat (ground cover and shade cover) between two populations occurring at different elevations. We assessed the heterogeneity of dietary and microhabitat resources within each population's environment by quantifying the availability of prey items, ground cover, and shade cover in each environment. Overall, our results demonstrate that despite differences in resource heterogeneity between elevations, resource selection did not consistently differ between populations. Moreover, environmental heterogeneity was not associated with generalization of resource use. The low-elevation site had a broader range of available prey items, yet lizards at the high-elevation site demonstrated more generalization in diet. In contrast, the high-elevation site had a broader range of available microhabitats, but the lizard populations at both sites were similarly generalized for shade cover selection and were similarly specialized for ground cover selection. Our results demonstrate that environmental heterogeneity of a particular resource does not necessarily predict the degree to which organisms specialize on that resource.

Evaluating outcomes of management targeting the recovery of a migratory songbird of conservation concern.

BACKGROUND: Assessing outcomes of habitat management is critical for informing and adapting conservation plans. From 2013-2019, a multi-stage management initiative, led by the American Bird Conservancy (ABC), aims to create >25,000 ha of shrubland and early-successional vegetation to benefit Golden-winged Warblers (Vermivora chrysoptera) in managed forested landscapes of the western Great Lakes region. We studied a dense breeding population of Golden-winged Warblers at Rice Lake National Wildlife Refuge (NWR) in Minnesota, USA, where ABC initiative management was implemented to benefit the species. METHODS: We monitored abundance before (2011-2014) and after (2015-2016) management, and we estimated full-season productivity (i.e., young recruited into the fall population) from predictive, spatially explicit models, informed by nest and fledgling survival data collected at sites in the western Great Lakes region, including Rice Lake NWR, during 2011 and 2012. Then, using biologically informed models of bird response to observed and predicted vegetation succession, we estimated the cumulative change in population recruitment over various scenarios of vegetation succession and demographic response. RESULTS: We observed an 32% decline in abundance of breeding pairs and estimated a 27% decline in per-pair full-season productivity following management, compared to no change in a nearby control site. In models that ranged from highly optimistic to progressively more realistic scenarios, we estimated a net loss of 72-460 juvenile Golden-winged Warblers produced from the managed site in the 10-20 years following management. Even if our well-informed and locally validated productivity models produced erroneous estimates and the management resulted in only a temporary reduction in abundance (i.e., no change in productivity), our forecast models still predicted a net loss of 137-260 juvenile Golden-winged Warblers from the managed area over the same time frame. CONCLUSIONS: Our study site represents only a small portion of a massive management initiative; however, the management at our site was conducted in accordance with the initiative's management plans, the resulting vegetation structure is consistent with that of other areas managed under the initiative, and those responsible for the initiative have described the management at our study site as successful Golden-winged Warbler management. Our assessment demonstrates that, at least for the only site for which pre- and post-management data on Golden-winged Warblers exist, the ABC management initiative is having a substantial and likely enduring negative impact on the species it purports to benefit. We suggest that incorporating region-specific, empirical information about Golden-winged Warbler-habitat relations into habitat management efforts would increase the likelihood of a positive response by Golden-winged Warblers.

Geolocator deployment reduces return rate, alters selection, and impacts demography in a small songbird.

In the past few years, miniature light-level geolocators have been developed for tracking wild bird species that were previously too small to track during their full annual cycle. Geolocators offer an exciting opportunity to study the full annual cycle for many species. However, the potential detrimental effects of carrying geolocators are still poorly understood, especially for small-bodied birds. Here, we deployed light-level geolocators on common yellowthroat warblers (Geothlypis trichas). Over two years, we monitored return rates and neighborhood demography for 40 warblers carrying a geolocator and 20 reference birds that did not carry a geolocator. We compared the two groups with long-term data from 108 unmanipulated birds breeding at the same location in previous and subsequent years. Overall, we found that individuals carrying a geolocator were less likely to return to the study site in the following year (21% to 33% returned, depending on inclusion criteria) than either contemporaneous controls (55%) or long-term controls (55%). Among birds marked with geolocators, we also detected viability selection for greater wing length, whereas this pattern was not present in control birds. Finally, in each year after geolocator deployment, inexperienced breeders colonized vacant territories and this demographic effect persisted for two years after deployment. Sexual selection and ornamentation are strongly age-dependent in this system, and behavioral data collected after geolocator deployment is likely to differ systematically from natural conditions. Clearly geolocators will continue to be useful tools, but we suggest that future studies should carefully consider the potential for biased returns and the ecological validity of behavioral data collected from geolocator marked populations.

Response to Lisovski et al.

Lisovski et al.[1] describe the widely recognized limitations of light-level geolocator data for identifying short-distance latitudinal movements, recommend that caution be used when interpreting such data, intimated that we did not use such caution and argued that environmental shading likely explained the Golden-winged Warbler (Vermivora chrysoptera) movements described in our 2015 report [2]. Lisovski et al.[1] conclude that the bird movements we reported could not be disentangled from estimation error in stationary animals caused by environmental shading. We argue that, to the contrary, these hypotheses can easily be disentangled because the premise that environmental shading caused synchronous and parallel error among geolocators is false. With their assertion that our location estimates could be biased by >3,500 km on a day with no observable local sources of shading, Lisovski et al.[1] have taken a position of incredulity toward all geolocator-based animal movement data published to date.

Tornadic storm avoidance behavior in breeding songbirds.

Migration is a common behavior used by animals of many taxa to occupy different habitats during different periods. Migrant birds are categorized as either facultative (i.e., those that are forced to migrate by some proximal cue, often weather) or obligate (i.e., those that migrate on a regular cycle). During migration, obligate migrants can curtail or delay flights in response to inclement weather or until favorable winds prevail, and they can temporarily reorient or reverse direction when ecological or meteorological obstacles are encountered. However, it is not known whether obligate migrants undertake facultative migrations and make large-scale movements in response to proximal cues outside of their regular migration periods. Here, we present the first documentation of obligate long-distance migrant birds undertaking a facultative migration, wherein breeding golden-winged warblers (Vermivora chrysoptera) carrying light-level geolocators performed a >1,500 km 5-day circumvention of a severe tornadic storm. The birds evacuated their breeding territories >24 hr before the arrival of the storm and atmospheric variation associated with it. The probable cue, radiating >1,000 km from tornadic storms, perceived by birds and influencing bird behavior and movements, is infrasound (i.e., sound below the range of human hearing). With the predicted increase in severity and frequency of similar storms as anthropogenic climate change progresses, understanding large-scale behavioral responses of animals to such events will be an important objective of future research.