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.

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.

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.

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.

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

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

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.

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.

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.

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.

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.