Ongoing introgression of a secondary sexual plumage trait in a stable avian hybrid zone.

Hybrid zones are dynamic systems where natural selection, sexual selection, and other evolutionary forces can act on reshuffled combinations of distinct genomes. The movement of hybrid zones, individual traits, or both are of particular interest for understanding the interplay between selective processes. In a hybrid zone involving two lek-breeding birds, secondary sexual plumage traits of Manacus vitellinus, including bright yellow collar and olive belly color, have introgressed asymmetrically ~50 km across the genomic center of the zone into populations more genetically similar to Manacus candei. Males with yellow collars are preferred by females and are more aggressive than parental M. candei, suggesting that sexual selection was responsible for the introgression of male traits. We assessed the spatial and temporal dynamics of this hybrid zone using historical (1989 - 1994) and contemporary (2017 - 2020) transect samples to survey both morphological and genetic variation. Genome-wide SNP data and several male phenotypic traits show that the genomic center of the zone has remained spatially stable, whereas the olive belly color of male M. vitellinus has continued to introgress over this time period. Our data suggest that sexual selection can continue to shape phenotypes dynamically, independent of a stable genomic transition between species.

Equivocal support for the climate variability hypothesis within a Neotropical bird assemblage.

The climate variability hypothesis posits that an organism's exposure to temperature variability determines the breadth of its thermal tolerance and has become an important framework for understanding variation in species' susceptibilities to climate change. For example, ectotherms from more thermally stable environments tend to have narrower thermal tolerances and greater sensitivity to projected climate warming. Among endotherms, however, the relationship between climate variability and thermal physiology is less clear, particularly with regard to microclimate variation-small-scale differences within or between habitats. To address this gap, we explored associations between two sources of temperature variation (habitat type and vertical forest stratum) and (1) thermal physiological traits and (2) temperature sensitivity metrics within a diverse assemblage of Neotropical birds (n = 89 species). We used long-term temperature data to establish that daily temperature regimes in open habitats and forest canopy were both hotter and more variable than those in the forest interior and forest understory, respectively. Despite these differences in temperature regime, however, we found little evidence that species' thermal physiological traits or temperature sensitivity varied in association with either habitat type or vertical stratum. Our findings provide two novel and important insights. First, and in contrast to the supporting empirical evidence from ectotherms, the thermal physiology of birds at our study site appears to be largely decoupled from local temperature variation, providing equivocal support for the climate variability hypothesis in endotherms. Second, we found no evidence that the thermal physiology of understory forest birds differed from that of canopy or open-habitat species-an oft-invoked, yet previously untested, mechanism for why these species are so vulnerable to environmental change.

Widespread Torpor Use in Hummingbirds from the Thermally Stable Lowland Tropics.

AbstractTorpor, the temporary reduction of metabolic rate and body temperature, is a common energy-saving strategy in endotherms. Because of their small body size and energetically demanding life histories, hummingbirds have proven useful for understanding when and why endotherms use torpor. Previous studies of torpor in hummingbirds have been largely limited to tropical montane species or long-distance migrants that regularly experience challenging thermal conditions. Comparatively little is known, however, about the use of torpor in hummingbirds of the lowland tropics, where relatively high and stable year-round temperatures may at least partially negate the need for torpor. To fill this knowledge gap, we tested for the occurrence of torpor in tropical lowland hummingbirds (n=37 individuals of six species) from central Panama. In controlled experimental conditions simulating the local temperature regime, all six species used torpor to varying degrees and entered torpor at high ambient temperatures (i.e., ≥28°C), indicating that hummingbirds from the thermally stable lowland tropics regularly use torpor. Torpor reduced overnight mass loss, with individuals that spent more time in torpor losing less body mass during temperature experiments. Body mass was the best predictor of torpor depth and duration among and within species-smaller species and individuals tended to use torpor more frequently and enter deeper torpor. Average mass loss in our experiments (∼8%-10%) was greater than that reported in studies of hummingbirds from higher elevation sites (∼4%). We therefore posit that the energetic benefits accrued from torpor may be limited by relatively high nighttime temperatures in the lowland tropics, although further studies are needed to test this hypothesis.

Multi-Year Comparison of Community- and Species-Level West Nile Virus Antibody Prevalence in Birds from Atlanta, Georgia and Chicago, Illinois, 2005-2016.

West Nile virus (WNV) is prevalent in the United States but shows considerable variation in transmission intensity. The purpose of this study was to compare patterns of WNV seroprevalence in avian communities sampled in Atlanta, Georgia and Chicago, Illinois during a 12-year period (Atlanta 2010-2016; Chicago 2005-2012) to reveal regional patterns of zoonotic activity of WNV. WNV antibodies were measured in wild bird sera using ELISA and serum neutralization methods, and seroprevalence among species, year, and location of sampling within each city were compared using binomial-distributed generalized linear mixed-effects models. Seroprevalence was highest in year-round and summer-resident species compared with migrants regardless of region; species explained more variance in seroprevalence within each city. Northern cardinals were the species most likely to test positive for WNV in each city, whereas all other species, on average, tested positive for WNV in proportion to their sample size. Despite similar patterns of seroprevalence among species, overall seroprevalence was higher in Atlanta (13.7%) than in Chicago (5%). Location and year of sampling had minor effects, with location explaining more variation in Atlanta and year explaining more variation in Chicago. Our findings highlight the nature and magnitude of regional differences in WNV urban ecology.

Long-term monitoring reveals widespread and severe declines of understory birds in a protected Neotropical forest.

Long-term studies on the population dynamics of tropical resident birds are few, and it remains poorly understood how their populations have fared in recent decades. Here, we analyzed a 44-y population study of a Neotropical understory bird assemblage from a protected forest reserve in central Panama to determine if and how populations have changed from 1977 to 2020. Using the number of birds captured in mist nets as an index of local abundance, we estimated trends over time for a diverse suite of 57 resident species that comprised a broad range of ecological and behavioral traits. Estimated abundances of 40 (∼70%) species declined over the sampling period, whereas only 2 increased. Furthermore, declines were severe: 35 of the 40 declining species exhibited large proportional losses in estimated abundance, amounting to ≥50% of their initial estimated abundances. Declines were largely independent of ecology (i.e., body mass, foraging guild, or initial abundance) or phylogenetic affiliation. These widespread, severe declines are particularly alarming, given that they occurred in a relatively large (∼22,000-ha) forested area in the absence of local fragmentation or recent land-use change. Our findings provide robust evidence of tropical bird declines in intact forests and bolster a large body of literature from temperate regions suggesting that bird populations may be declining at a global scale. Identifying the ecological mechanisms underlying these declines should be an urgent conservation priority.

Early-life patterns of growth are linked to levels of phenotypic trait covariance and postfledging mortality across avian species.

Life history studies have established that trade-offs between growth and survival are common both within and among species. Identifying the factor(s) that mediate this trade-off has proven difficult, however, especially at the among-species level. In this study, we examined a series of potentially interrelated traits in a community of temperate-zone passerine birds to help understand the putative causes and consequences of variation in early-life growth among species. First, we examined whether nest predation risk (a proven driver of interspecific variation in growth and development rates) was correlated with species-level patterns of incubation duration and nestling period length. We then assessed whether proxies for growth rate covaried with mean trait covariance strength (i.e., phenotypic correlations ( rp), which can be a marker of early-life stress) among body mass, tarsus length, and wing length at fledging. Finally, we examined whether trait covariance strength at fledging was related to postfledging survival. We found that higher nest predation risk was correlated with faster skeletal growth and that our proxies for growth corresponded with increased trait covariance strength ( rp), which subsequently, correlated with higher mortality in the next life stage (postfledging period). These results provide an indication that extrinsic pressures (nest predation) impact rates of growth, and that there are costs of rapid growth across species, expressed as higher mean rp and elevated postfledging mortality. The link between higher levels of trait covariance at fledging and increased mortality is unclear, but increased trait covariance strength may reflect reduced phenotypic flexibility (i.e., phenotypic canalization), which may limit an organism's capacity for coping with environmental or ecological variability.

Cost-Reducing Traits for Agonistic Head Collisions: A Case for Neurophysiology.

Many animal species have evolved extreme behaviors requiring them to engage in repeated high-impact collisions. These behaviors include mating displays like headbutting in sheep and drumming in woodpeckers. To our knowledge, these taxa do not experience any notable acute head trauma, even though the deceleration forces would cause traumatic brain injury in most animals. Previous research has focused on skeletomuscular morphology, biomechanics, and material properties in an attempt to explain how animals moderate these high-impact forces. However, many of these behaviors are understudied, and most morphological or computational studies make assumptions about the behavior without accounting for the physiology of an organism. Studying neurophysiological and immune adaptations that covary with these behaviors can highlight unique or synergistic solutions to seemingly deleterious behavioral displays. Here, we argue that selection for repeated, high-impact head collisions may rely on a suite of coadaptations in intracranial physiology as a cost-reducing mechanism. We propose that there are three physiological systems that could mitigate the effects of repeated head trauma: (1) the innate neuroimmune response; (2) the glymphatic system, and (3) the choroid plexus. These systems are interconnected yet can evolve in an independent manner. We then briefly describe the function of these systems, their role in head trauma, and research that has examined how these systems may evolve to help reduce the cost of repeated, forceful head impacts. Ultimately, we note that little is known about cost-reducing intracranial mechanisms making it a novel field of comparative study that is ripe for exploration.

Parental benefits and offspring costs reflect parent-offspring conflict over the age of fledging among songbirds.

Parent-offspring conflict has explained a variety of ecological phenomena across animal taxa, but its role in mediating when songbirds fledge remains controversial. Specifically, ecologists have long debated the influence of songbird parents on the age of fledging: Do parents manipulate offspring into fledging to optimize their own fitness or do offspring choose when to leave? To provide greater insight into parent-offspring conflict over fledging age in songbirds, we compared nesting and postfledging survival rates across 18 species from eight studies in the continental United States. For 12 species (67%), we found that fledging transitions offspring from comparatively safe nesting environments to more dangerous postfledging ones, resulting in a postfledging bottleneck. This raises an important question: as past research shows that offspring would benefit-improve postfledging survival-by staying in the nest longer: Why then do they fledge so early? Our findings suggest that parents manipulate offspring into fledging early for their own benefit, but at the cost of survival for each individual offspring, reflecting parent-offspring conflict. Early fledging incurred, on average, a 13.6% postfledging survival cost for each individual offspring, but parents benefitted through a 14.0% increase in the likelihood of raising at least one offspring to independence. These parental benefits were uneven across species-driven by an interaction between nest mortality risk and brood size-and predicted the age of fledging among species. Collectively, our results suggest that parent-offspring conflict and associated parental benefits explain variation in fledging age among songbird species and why postfledging bottlenecks occur.

Hygric Niches for Tropical Endotherms.

Biotic selective pressures dominate explanations for the evolutionary ecology of tropical endotherms. Yet, abiotic factors, principally precipitation regimes, shape biogeographical and phenological patterns in tropical regions. Despite its importance, we lack a framework for understanding when, why, and how rain affects endotherms. Here, we review how tropical birds and mammals respond to rain at individual, population, and community levels, and propose a conceptual framework to interpret divergent responses. Diverse direct and indirect mechanisms underlie responses to rainfall, including physiological, top-down, and food-related drivers. Our framework constitutes a roadmap for the empirical studies required to understand the consequences of rainfall variability. Identifying the patterns and mechanisms underpinning responses to temporal variation in precipitation is crucial to anticipate consequences of anthropogenic climate change.

Haemosporidian Parasite Infections In the Dickcissel ( Spiza americana): Prevalence and Costs.

Haemosporidian parasites are widespread in birds and are commonly used to evaluate ecological, evolutionary, and behavioral consequences of pathogen infection. While haemosporidian parasites may be important agents of selection, information on the incidence and outcomes of infection in many wild birds remains incomplete and warrants further inquiry. We examined the prevalence and costs of haemosporidian parasites in a wild population of dickcissels ( Spiza americana; n = 170) breeding in central Illinois. Over 2 breeding seasons, prevalence of haemosporidian parasites was 41% and was similar between sexes and years. Within each sex, there was no association between proxies of fitness (body condition and number of fledglings produced) and infection status. While we found no evidence that haemosporidian parasites have a direct, negative impact on dickcissels, we discuss how extra-pair paternity and changes across the life cycle of dickcissels and haemosporidian parasites may have masked or prevented detection of negative effects in our study. Ultimately our findings contribute to a growing literature providing improved clarity on how and when parasite infections can negatively impact wild host organisms and can aid in guiding future work examining such associations.

Selective constraint and adaptive potential of West Nile virus within and among naturally infected avian hosts and mosquito vectors.

Arthropod-borne viruses are among the most genetically constrained RNA viruses, yet they have a remarkable propensity to adapt and emerge. We studied wild birds and mosquitoes naturally infected with West Nile virus (WNV) in a 'hot spot' of virus transmission in Chicago, IL, USA. We generated full coding WNV genome sequences from spatiotemporally matched bird and mosquito samples using high-throughput sequencing, allowing a molecular evolutionary assessment with deep coverage. Mean FST among samples was 0.66 (±0.02 SE) and was bimodal, with mean nucleotide diversity being higher between samples (interhost πN = 0.001; πS = 0.024) than within them (intrahost πN < 0.0001; πS < 0.001). Eight genomic sites with FST > 1.01 (in the PrM, NS2a, NS3, NS4b, and 5'-noncoding genomic regions) showed bird versus mosquito variant frequency differences of >30 per cent and/or polymorphisms fixed in ≥5 host or vector individuals, suggesting host tropism for these variants. However, phylogenetic analyses demonstrated a lack of grouping by bird or mosquito, most inter-sample differences were synonymous (mean interhost πN/πS = 0.04), and there was no significant difference between hosts and vectors in either their nucleotide diversities or levels of purifying selection (mean intrahost πN/πS = 0.28 in birds and πN/πS = 0.21 in mosquitoes). This finding contrasts with the 'trade-off' and 'selective sieve' hypotheses that have been proposed and tested in the laboratory, which predict strong host versus vector effects on WNV genetic variation, with heightened selective constraint in birds alternating with heightened viral diversity in mosquitoes. Overall, our data show WNV to be highly selectively constrained within and between both hosts and vectors but still able to vary at a limited number of sites across the genome. Such site-specific plasticity in the face of overall selective constraint may offer a mechanism whereby highly constrained viruses such as WNV and its relatives can still adapt and emerge.

Culex Flavivirus During West Nile Virus Epidemic and Interepidemic Years in Chicago, United States.

Culex flavivirus (CxFV) is an insect-specific flavivirus infecting Culex mosquitoes, which are important vectors of West Nile virus (WNV). CxFV and WNV cocirculate in nature and coinfect Culex mosquitoes, including in a WNV "hotspot" in suburban Chicago. We previously identified a positive association between CxFV and WNV in mosquito pools collected from suburban Chicago in 2006. To further investigate this phenomenon, we compared the spatial and temporal distribution of CxFV during an interepidemic year (2011) and an epidemic year (2012) for WNV. Both viruses were more prevalent in mosquito pools in 2012 compared to 2011. During both years, the CxFV infection status of mosquito pools was associated with environmental factors such as habitat type and precipitation frequency rather than coinfection with WNV. These results support the idea that WNV and CxFV are ecologically associated, perhaps because both viruses respond to similar environmental drivers of mosquito populations.

Overlap in the Seasonal Infection Patterns of Avian Malaria Parasites and West Nile Virus in Vectors and Hosts.

Multiple vector-borne pathogens often circulate in the same vector and host communities, and seasonal infection dynamics influence the potential for pathogen interactions. Here, we explore the seasonal infection patterns of avian malaria (Haemosporida) parasites (Plasmodium and Haemoproteus) and West Nile virus (WNV) in birds and mosquitoes in suburban Chicago. We show that both pathogens vary seasonally in Culex mosquitoes and avian hosts, but that patterns of covariation are complex. Different putative Plasmodium species varied asynchronously across the season in mosquitoes and birds, suggesting that different forces may govern their transmission. Infections of Culex mosquitoes with Plasmodium parasites were positively associated with WNV infections in pools of individuals aggregated from the same time and site, suggesting that these pathogens respond to common environmental drivers and co-circulate among the same host and vector populations. Future research should focus on these common drivers, and whether these pathogens interact in vectors and hosts.

Plasmodium prevalence across avian host species is positively associated with exposure to mosquito vectors.

The prevalence of vector-borne parasites varies greatly across host species, and this heterogeneity has been used to relate infectious disease susceptibility to host species traits. However, a few empirical studies have directly associated vector-borne parasite prevalence with exposure to vectors across hosts. Here, we use DNA sequencing of blood meals to estimate utilization of different avian host species by Culex mosquitoes, and relate utilization by these malaria vectors to avian Plasmodium prevalence. We found that avian host species that are highly utilized as hosts by avian malaria vectors are significantly more likely to have Plasmodium infections. However, the effect was not consistent among individual Plasmodium taxa. Exposure to vector bites may therefore influence the relative number of all avian Plasmodium infections among host species, while other processes, such as parasite competition and host-parasite coevolution, delimit the host distributions of individual Plasmodium species. We demonstrate that links between avian malaria susceptibility and host traits can be conditioned by patterns of exposure to vectors. Linking vector utilization rates to host traits may be a key area of future research to understand mechanisms that produce variation in the prevalence of vector-borne pathogens among host species.

Identification of Avian and Hemoparasite DNA in Blood-Engorged Abdomens of Culex pipiens (Diptera; Culicidae) from a West Nile Virus Epidemic region in Suburban Chicago, Illinois.

Multiple mosquito-borne parasites cocirculate in nature and potentially interact. To understand the community of parasites cocirculating with West Nile virus (WNV), we screened the bloodmeal content of Culex pipiens L. mosquitoes for three common types of hemoparasites. Blood-fed Cx. pipiens were collected from a WNV-epidemic area in suburban Chicago, IL, from May to September 2005 through 2010. DNA was extracted from dissected abdomens and subject to PCR and direct sequencing to identify the vertebrate host. RNA was extracted from the head or thorax and screened for WNV using quantitative reverse transcriptase PCR. Seventy-nine engorged females with avian host origin were screened using PCR and amplicon sequencing for filarioid nematodes, Haemosporida, and trypanosomatids. Filarioid nematodes were identified in 3.8% of the blooded abdomens, Plasmodium sp. in 8.9%, Haemoproteus in 31.6%, and Trypanosoma sp. in 6.3%. The sequences from these hemoparasite lineages were highly similar to sequences from birds in prior studies in suburban Chicago. Overall, 50.6% of blood-fed Culex pipiens contained hemoparasite DNA in their abdomen, presumably from current or prior bloodmeals. Additionally, we detected hemoparasite DNA in the blooded abdomen of three of 10 Cx. pipiens infected with WNV.

WEST NILE VIRUS ANTIBODY DECAY RATE IN FREE-RANGING BIRDS.

Antibody duration, following a humoral immune response to West Nile virus (WNV) infection, is poorly understood in free-ranging avian hosts. Quantifying antibody decay rate is important for interpreting serologic results and for understanding the potential for birds to serorevert and become susceptible again. We sampled free-ranging birds in Chicago, Illinois, US, from 2005 to 2011 and Atlanta, Georgia, US, from 2010 to 2012 to examine the dynamics of antibody decay following natural WNV infection. Using serial dilutions in a blocking enzyme-linked immunosorbent assay, we quantified WNV antibody titer in repeated blood samples from individual birds over time. We quantified a rate of antibody decay for 23 Northern Cardinals (Cardinalis cardinalis) of 0.198 natural log units per month and 24 individuals of other bird species of 0.178 natural log units per month. Our results suggest that juveniles had a higher rate of antibody decay than adults, which is consistent with nonlinear antibody decay at different times postexposure. Overall, most birds had undetectable titers 2 yr postexposure. Nonuniform WNV antibody decay rates in free-ranging birds underscore the need for cautious interpretation of avian serology results in the context of arbovirus surveillance and epidemiology.

Host group formation decreases exposure to vector-borne disease: a field experiment in a 'hotspot' of West Nile virus transmission.

Animals can decrease their individual risk of predation by forming groups. The encounter-dilution hypothesis extends the potential benefits of gregariousness to biting insects and vector-borne disease by predicting that the per capita number of insect bites should decrease within larger host groups. Although vector-borne diseases are common and can exert strong selective pressures on hosts, there have been few tests of the encounter-dilution effect in natural systems. We conducted an experimental test of the encounter-dilution hypothesis using the American robin (Turdus migratorius), a common host species for the West Nile virus (WNV), a mosquito-borne pathogen. By using sentinel hosts (house sparrows, Passer domesticus) caged in naturally occurring communal roosts in the suburbs of Chicago, we assessed sentinel host risk of WNV exposure inside and outside of roosts. We also estimated per capita host exposure to infected vectors inside roosts and outside of roosts. Sentinel birds caged inside roosts seroconverted to WNV more slowly than those outside of roosts, suggesting that social groups decrease per capita exposure to infected mosquitoes. These results therefore support the encounter-dilution hypothesis in a vector-borne disease system. Our results suggest that disease-related selective pressures on sociality may depend on the mode of disease transmission.

An inverse association between West Nile virus serostatus and avian malaria infection status.

BACKGROUND: Various ecological and physiological mechanisms might influence the probability that two or more pathogens may simultaneously or sequentially infect a host individual. Concurrent infections can have important consequences for host condition and fitness, including elevated mortality risks. In addition, interactions between coinfecting pathogens may have important implications for transmission dynamics. METHODS: Here, we explore patterns of association between two common avian pathogens (West Nile virus and avian malaria parasites) among a suburban bird community in Chicago, IL, USA that share mosquito vectors. We surveyed 1714 individual birds across 13 species for both pathogens through established molecular protocols. RESULTS: Field investigations of haemosporidian and West Nile virus (WNV) infections among sampled birds yielded an inverse association between WNV serostatus and Plasmodium infection status. This relationship occurred in adult birds but not in juveniles. There was no evidence for a relationship between Haemoproteus infection and WNV serostatus. We detected similar prevalence of Plasmodium among birds captured with active WNV infections and spatiotemporally paired WNV-naïve individuals of the same species, demonstrating that the two pathogens can co-infect hosts. CONCLUSIONS: Mechanisms explaining the negative association between WNV serostatus and Plasmodium infection status remain unclear and must be resolved through experimental infection procedures. However, our results highlight potential interactions between two common avian pathogens that may influence their transmission among hosts. This is especially relevant considering that West Nile virus is a common zoonotic pathogen with public health implications. Moreover, both pathogens are instructive models in infectious disease ecology, and infection with either has fitness consequences for their avian hosts.

Dispersal of adult culex mosquitoes in an urban west nile virus hotspot: a mark-capture study incorporating stable isotope enrichment of natural larval habitats.

Dispersal is a critical life history behavior for mosquitoes and is important for the spread of mosquito-borne disease. We implemented the first stable isotope mark-capture study to measure mosquito dispersal, focusing on Culex pipiens in southwest suburban Chicago, Illinois, a hotspot of West Nile virus (WNV) transmission. We enriched nine catch basins in 2010 and 2011 with 15N-potassium nitrate and detected dispersal of enriched adult females emerging from these catch basins using CDC light and gravid traps to distances as far as 3 km. We detected 12 isotopically enriched pools of mosquitoes out of 2,442 tested during the two years and calculated a mean dispersal distance of 1.15 km and maximum flight range of 2.48 km. According to a logistic distribution function, 90% of the female Culex mosquitoes stayed within 3 km of their larval habitat, which corresponds with the distance-limited genetic variation of WNV observed in this study region. This study provides new insights on the dispersal of the most important vector of WNV in the eastern United States and demonstrates the utility of stable isotope enrichment for studying the biology of mosquitoes in other disease systems.