ABSTRACT
Microscopic symbionts represent crucial links in biological communities. However, they present technical challenges in high-throughput sequencing (HTS) studies due to their small size and minimal high-quality DNA yields, hindering our understanding of host-symbiont coevolution at microevolutionary and macroevolutionary scales. One approach to overcome those barriers is to pool multiple individuals from the same infrapopulation (i.e., individual host) and sequence them together (Pool-Seq), but individual-level information is then compromised. To simultaneously address both issues (i.e., minimal DNA yields and loss of individual-level information), we implemented a strategic Pool-Seq approach to assess variation in sequencing performance and categorize genetic diversity (single nucleotide polymorphisms (SNPs)) at both the individual-level and infrapopulation-level for microscopic feather mites. To do so, we collected feathers harboring mites (Proctophyllodidae: Amerodectes protonotaria) from four individual Prothonotary Warblers (Parulidae: Protonotaria citrea). From each of the four hosts (i.e., four mite infrapopulations), we conducted whole-genome sequencing on three extraction pools consisting of different numbers of mites (1 mite, 5 mites, and 20 mites). We found that samples containing pools of multiple mites had more sequencing reads map to the feather mite reference genome than did the samples containing only a single mite. Mite infrapopulations were primarily genetically structured by their associated individual hosts (not pool size) and the majority of SNPs were shared by all pools within an infrapopulation. Together, these results suggest that the patterns observed are driven by evolutionary processes occurring at the infrapopulation level and are not technical signals due to pool size. In total, despite the challenges presented by microscopic symbionts in HTS studies, this work highlights the value of both individual-level and infrapopulation-level sequencing toward our understanding of host-symbiont coevolution at multiple evolutionary scales.
ABSTRACT
Researchers often examine symbiont host specificity as a species-level pattern, but it can also be key to understanding processes occurring at the population level, which are not as well understood. The specialist-generalist variation hypothesis (SGVH) attempts to explain how host specificity influences population-level processes, stating that single-host symbionts (specialists) exhibit stronger population genetic structure than multi-host symbionts (generalists) because of fewer opportunities for dispersal and more restricted gene flow between populations. However, this hypothesis has not been tested in systems with highly mobile hosts, in which population connectivity may vary temporally and spatially. To address this gap, we tested the SGVH on proctophyllodid feather mites found on migratory warblers (family Parulidae) with contrasting host specificities, Amerodectes protonotaria (a host specialist of Protonotaria citrea) and A. ischyros (a host generalist of 17 parulid species). We used a pooled-sequencing approach and a novel workflow to analyse genetic variants obtained from whole genome data. Both mite species exhibited fairly weak population structure overall, and contrary to predictions of the SGVH, the generalist was more strongly structured than the specialist. These results may suggest that specialists disperse more freely among conspecifics, whereas generalists sort according to geography. Furthermore, our results may reflect an unexpected period for mite transmission - during the nonbreeding season of migratory hosts - as mite population structure more closely reflects the distributions of hosts during the nonbreeding season. Our findings alter our current understanding of feather mite biology and highlight the potential for studies to explore factors driving symbiont diversification at multiple evolutionary scales.
Subject(s)
Mites , Passeriformes , Animals , Mites/genetics , Passeriformes/genetics , Biological Evolution , Host Specificity , Geography , Symbiosis/geneticsABSTRACT
A fundamental aspect of symbiotic relationships is host specificity, ranging from extreme specialists associated with only a single host species to generalists associated with many different species. Although symbionts with limited dispersal capabilities are expected to be host specialists, some are able to associate with multiple hosts. Understanding the micro- and macro-evolutionary causes of variations in host specificity is often hindered by sampling biases and the limited power of traditional evolutionary markers. Here, we studied feather mites to address the barriers associated with estimates of host specificity for dispersal-limited symbionts. We sampled feather mites (Proctophyllodidae) from a nearly comprehensive set of North American breeding warblers (Parulidae) to study mite phylogenetic relationships and host-symbiont codiversification. We used pooled-sequencing (Pool-Seq) and short-read Illumina technology to interpret results derived from a traditional barcoding gene (cytochrome c oxidase subunit 1) versus 11 protein-coding mitochondrial genes using concatenated and multispecies coalescent approaches. Despite the statistically significant congruence between mite and host phylogenies, mite-host specificity varies widely, and host switching is common regardless of the genetic marker resolution (i.e., barcode vs. multilocus). However, the multilocus approach was more effective than the single barcode in detecting the presence of a heterogeneous Pool-Seq sample. These results suggest that presumed symbiont dispersal capabilities are not always strong indicators of host specificity or of historical host-symbiont coevolutionary events. A comprehensive sampling at fine phylogenetic scales may help to better elucidate the microevolutionary filters that impact macroevolutionary processes regulating symbioses, particularly for dispersal-limited symbionts. [Codiversification; cophylogenetics; feather mites; host switching; pooled sequencing; species delineation; symbiosis, warblers.].
Subject(s)
Host Specificity , Mites , Animals , Phylogeny , Mites/genetics , Biological Evolution , SymbiosisABSTRACT
Feather mites are ubiquitous, permanent, obligate ectosymbionts of avian hosts and are a valuable natural system for studying host-symbiont evolutionary and ecological dynamics at multiple levels of biological organization. However, a lack of a sequenced genome impedes molecular studies using this system. Therefore, we present the first draft genome of a symbiotic feather mite, Amerodectes protonotaria Hernandes 2018. The genome sequence data presented here were derived from an individual female mite that was collected in the field from Protonotaria citrea, its only known host species. Short read sequence data were obtained using an Illumina NovaSeq 6000 platform. From these data, we assembled a 59,665,063 bp draft genome consisting of 2,399 contigs. Raw short reads and the assembled genome sequence are available at the National Center for Biotechnology Information (NCBI)'s Sequence Read Archive (SRA) under BioProject PRJNA884722. The data presented here are beneficial for future research on the biology and evolution of closely related mites and the genomics of host-symbiont interactions.
ABSTRACT
The Prothonotary Warbler (Protonotaria citrea) is a nearctic-neotropical migratory songbird that breeds in forested swamps and riparian areas in the eastern-central United States and southern Ontario. It is the sole eastern North American wood-warbler that nests in cavities, the only species in the genus Protonotaria, and is one of the few hole-nesting hosts of the Brown-headed Cowbird (Molothrus ater), an obligate brood parasite. We present the whole genome sequence of this wood-warbler species. Illumina sequencing was performed on a genetic sample from a single female individual. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data is publicly available via Genbank: Sequence Read Archive (SRR19579445) and Assembly (JAOYNP000000000).
ABSTRACT
For many avian species, spatial migration patterns remain largely undescribed, especially across hemispheric extents. Recent advancements in tracking technologies and high-resolution species distribution models (i.e., eBird Status and Trends products) provide new insights into migratory bird movements and offer a promising opportunity for integrating independent data sources to describe avian migration. Here, we present a three-stage modeling framework for estimating spatial patterns of avian migration. First, we integrate tracking and band re-encounter data to quantify migratory connectivity, defined as the relative proportions of individuals migrating between breeding and nonbreeding regions. Next, we use estimated connectivity proportions along with eBird occurrence probabilities to produce probabilistic least-cost path (LCP) indices. In a final step, we use generalized additive mixed models (GAMMs) both to evaluate the ability of LCP indices to accurately predict (i.e., as a covariate) observed locations derived from tracking and band re-encounter data sets versus pseudo-absence locations during migratory periods and to create a fully integrated (i.e., eBird occurrence, LCP, and tracking/band re-encounter data) spatial prediction index for mapping species-specific seasonal migrations. To illustrate this approach, we apply this framework to describe seasonal migrations of 12 bird species across the Western Hemisphere during pre- and postbreeding migratory periods (i.e., spring and fall, respectively). We found that including LCP indices with eBird occurrence in GAMMs generally improved the ability to accurately predict observed migratory locations compared to models with eBird occurrence alone. Using three performance metrics, the eBird + LCP model demonstrated equivalent or superior fit relative to the eBird-only model for 22 of 24 species-season GAMMs. In particular, the integrated index filled in spatial gaps for species with over-water movements and those that migrated over land where there were few eBird sightings and, thus, low predictive ability of eBird occurrence probabilities (e.g., Amazonian rainforest in South America). This methodology of combining individual-based seasonal movement data with temporally dynamic species distribution models provides a comprehensive approach to integrating multiple data types to describe broad-scale spatial patterns of animal movement. Further development and customization of this approach will continue to advance knowledge about the full annual cycle and conservation of migratory birds.
Subject(s)
Animal Migration , Birds , Animals , Seasons , South AmericaABSTRACT
Collisions with buildings cause up to 1 billion bird fatalities annually in the United States and Canada. However, efforts to reduce collisions would benefit from studies conducted at large spatial scales across multiple study sites with standardized methods and consideration of species- and life-history-related variation and correlates of collisions. We addressed these research needs through coordinated collection of data on bird collisions with buildings at sites in the United States (35), Canada (3), and Mexico (2). We collected all carcasses and identified species. After removing records for unidentified carcasses, species lacking distribution-wide population estimates, and species with distributions overlapping fewer than 10 sites, we retained 269 carcasses of 64 species for analysis. We estimated collision vulnerability for 40 bird species with ≥2 fatalities based on their North American population abundance, distribution overlap in study sites, and sampling effort. Of 10 species we identified as most vulnerable to collisions, some have been identified previously (e.g., Black-throated Blue Warbler [Setophaga caerulescens]), whereas others emerged for the first time (e.g., White-breasted Nuthatch [Sitta carolinensis]), possibly because we used a more standardized sampling approach than past studies. Building size and glass area were positively associated with number of collisions for 5 of 8 species with enough observations to analyze independently. Vegetation around buildings influenced collisions for only 1 of those 8 species (Swainson's Thrush [Catharus ustulatus]). Life history predicted collisions; numbers of collisions were greatest for migratory, insectivorous, and woodland-inhabiting species. Our results provide new insight into the species most vulnerable to building collisions, making them potentially in greatest need of conservation attention to reduce collisions and into species- and life-history-related variation and correlates of building collisions, information that can help refine collision management.
Correlaciones de las Colisiones de Aves contra Edificios en Tres Países de América del Norte Resumen Las colisiones contra los edificios causan hasta mil millones de fatalidades de aves al año en los Estados Unidos y en Canadá. Sin embargo, los esfuerzos por reducir estas colisiones se beneficiarían con estudios realizados a grandes escalas espaciales en varios sitios de estudio con métodos estandarizados y considerando las variaciones relacionadas a la historia de vida y a la especie y las correlaciones de las colisiones. Abordamos estas necesidades de investigación por medio de una recolección coordinada de datos sobre las colisiones de aves contra edificios en los Estados Unidos (35), Canadá (3) y México (2). Recolectamos todos los cadáveres y los identificamos hasta especie. Después de retirar los registros de cadáveres no identificados, las especies sin estimaciones poblacionales a nivel distribución y las especies con distribuciones traslapadas en menos de diez sitios, nos quedamos con 269 cadáveres de 64 especies para el análisis. Estimamos la vulnerabilidad a colisiones para 40 especies con ≥2 fatalidades con base en la abundancia poblacional para América del Norte, el traslape de su distribución entre los sitios de estudio y el esfuerzo de muestreo. De las diez especies que identificamos como las más vulnerables a las colisiones, algunas han sido identificadas previamente (Setophaga caerulescens), y otras aparecieron por primera vez (Sitta carolinensis), posiblemente debido a que usamos una estrategia de muestreo más estandarizada que en los estudios previos. El tamaño del edificio y el área del vidrio estuvieron asociados positivamente con el número de colisiones para cinco de ocho especies con suficientes observaciones para ser analizadas independientemente. La vegetación alrededor de los edificios influyó sobre las colisiones solamente para una de esas ocho especies Catharus ustulatus). Las historias de vida pronosticaron las colisiones; el número de colisiones fue mayor para las especies migratorias, insectívoras y aquellas que habitan en las zonas boscosas. Nuestros resultados proporcionan una nueva perspectiva hacia las especies más vulnerables a las colisiones contra edificios, lo que las pone en una necesidad potencialmente mayor de atención conservacionista para reducir estas colisiones y de estudio de las variaciones relacionadas con la especie y la historia de vida y las correlaciones de las colisiones contra edificios, información que puede ayudar a refinar el manejo de colisiones.
Subject(s)
Conservation of Natural Resources , Songbirds , Animals , Canada , Mexico , North America , United StatesABSTRACT
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.
Subject(s)
Behavior, Animal , Songbirds , Animals , Nesting BehaviorABSTRACT
Bergmann's rule is a well-established, ecogeographical principle that states that body size varies positively with latitude, reflecting the thermoregulatory benefits of larger bodies as temperatures decline. However, this principle does not seem to easily apply to migratory species that are able to avoid the extreme temperatures during winter at higher latitudes. Further, little is known about the ontogeny of this relationship across life stages or how it is influenced by ongoing global climate change. To address these knowledge gaps, we assessed the contemporary relationship between latitude and body size in a long-distance migratory species, the prothonotary warbler (Protonotaria citrea) across life stages (egg to adult) on their breeding grounds. We also measured historic eggs (1865-1961) to assess if the relationship between latitude and size during this life stage has changed over time. In accordance with Bergmann's rule, we found a positive relationship between latitude and body mass during all post-embryonic life stages, from early nestling stage through adulthood. We observed this same predicted pattern with historic eggs, but contemporary eggs exhibited the reverse (negative) relationship. We suggest that these results indicate a genetic component to this pattern and speculate that selection for larger body size in altricial nestlings as latitude increases may possibly drive the pattern in migratory species as even rare extreme cold weather events may cause mortality during early life stages. Furthermore, the opposite relationships observed in eggs, dependent on time period, may be related to the rapidly warming environments of higher latitudes that is associated with climate change. Although it is unclear what mechanism(s) would allow for this recent reversal in eggs (but still allow for its maintenance in later life stages). This evidence of a reversal suggests that anthropogenic climate change may be in the process of altering one of the longest-standing principles in ecology.
ABSTRACT
Understanding migratory connectivity is essential for determining the drivers behind population dynamics and for implementing effective conservation strategies for migratory species. Genetic markers provide a means to describe migratory connectivity; however, they can be uninformative for species with weak population genetic structure, which has limited their application. Here, we demonstrated a genomic approach to describing migratory connectivity in the prothonotary warbler, Protonotaria citrea, a Neotropical songbird of conservation concern. Using 26,189 single nucleotide polymorphisms (SNPs), we revealed regional genetic structure between the Mississippi River Valley and the Atlantic Seaboard with overall weak genetic differentiation among populations (FST = 0.0055; 95% CI: 0.0051-0.0059). Genetic variation had a stronger association with geographic rather than environmental factors, with each explaining 14.5% and 8.2% of genetic variation, respectively. By varying the numbers of genomic markers used in population assignment models with individuals of known provenance, we identified a maximum assignment accuracy (89.7% to site, 94.3% to region) using a subset of 600 highly differentiated SNPs. We then assigned samples from nonbreeding sites to breeding region and found low migratory connectivity. Our results highlight the importance of filtering markers for informative loci in models of population assignment. Quantifying migratory connectivity for weakly structured species will be useful for expanding studies to a wider range of migratory species across taxonomic groups and may contribute to a deeper understanding of the evolution of migratory strategies.
Subject(s)
Animal Migration/physiology , Genetics, Population , Songbirds/physiology , Animals , Genetic Variation , Louisiana , Models, Genetic , North Carolina , Polymorphism, Single Nucleotide , Principal Component Analysis , Reproducibility of Results , Songbirds/geneticsABSTRACT
Feather mites are obligatory ectosymbionts of birds that primarily feed on the oily secretions from the uropygial gland. Feather mite abundance varies within and among host species and has various effects on host condition and fitness, but there is little consensus on factors that drive variation of this symbiotic system. We tested hypotheses regarding how within-species and among-species traits explain variation in both (1) mite abundance and (2) relationships between mite abundance and host body condition and components of host fitness (reproductive performance and apparent annual survival). We focused on two closely related (Parulidae), but ecologically distinct, species: Setophaga cerulea (Cerulean Warbler), a canopy dwelling open-cup nester, and Protonotaria citrea (Prothonotary Warbler), an understory dwelling, cavity nester. We predicted that feather mites would be more abundant on and have a more parasitic relationship with P. citrea, and within P. citrea, females and older individuals would harbor greater mite abundances. We captured, took body measurements, quantified feather mite abundance on individuals' primaries and rectrices, and monitored individuals and their nests to estimate fitness. Feather mite abundance differed by species, but in the opposite direction of our prediction. There was no relationship between mite abundance and any measure of body condition or fitness for either species or sex (also contrary to our predictions). Our results suggest that species biology and ecological context may influence mite abundance on hosts. However, this pattern does not extend to differential effects of mites on measures of host body condition or fitness.
ABSTRACT
In migratory species, breeding and non-breeding locations are geographically separate, yet the effects of conditions from one stage may carry over to affect a subsequent stage. Ideally, to understand the mechanisms and implications of 'carry-over effects', one would need to follow individuals throughout the year, quantify potential environmental causal factors and physiological mediators during multiple life-history stages, and measure downstream fitness. Owing to current limitations of tracking technology, this is impossible for small, long-distance migrants, so indirect methods to characterize carry-over effects are required. Corticosterone (CORT) is a suspected physiological mediator of carry-over effects, but when collected from blood it provides only a physiological snapshot at that point in time. When extracted from feathers, however, feather corticosterone (CORTf) provides a measure of responses to stressors from previous, and longer, time periods. We collected feathers grown during two life-history stages (post-breeding and subsequent wintering) from individuals of two age classes of a rapidly declining migratory songbird, the cerulean warbler (Setophaga cerulea), on their breeding grounds and quantified CORTf concentrations. We then monitored reproduction and survival of individuals and analysed relationships among CORTf and age, body condition and future fitness. Compared with older males, second-year males had higher CORTf concentrations during both stages. When controlling for age and year, body condition at capture was positively related to CORTf concentrations from winter (especially for older birds). However, we found no relationships between CORTf and fitness (as defined by reproduction and survival). Thus, elevated CORT may represent a beneficial physiological response (e.g. hyperphagia prior to migration), particularly for certain life-history stages, and may mediate the condition in which individuals transition between stages. But for those birds that survive migration, subsequent fitness is likely determined by more recent events and local conditions (i.e. on breeding grounds), which have the potential to counteract conditions from the winter.
ABSTRACT
Forest cover in the eastern United States has increased over the past century and while some late-successional species have benefited from this process as expected, others have experienced population declines. These declines may be in part related to contemporary reductions in small-scale forest interior disturbances such as fire, windthrow, and treefalls. To mitigate the negative impacts of disturbance alteration and suppression on some late-successional species, strategies that emulate natural disturbance regimes are often advocated, but large-scale evaluations of these practices are rare. Here, we assessed the consequences of experimental disturbance (using partial timber harvest) on a severely declining late-successional species, the cerulean warbler (Setophaga cerulea), across the core of its breeding range in the Appalachian Mountains. We measured numerical (density), physiological (body condition), and demographic (age structure and reproduction) responses to three levels of disturbance and explored the potential impacts of disturbance on source-sink dynamics. Breeding densities of warblers increased one to four years after all canopy disturbances (vs. controls) and males occupying territories on treatment plots were in better condition than those on control plots. However, these beneficial effects of disturbance did not correspond to improvements in reproduction; nest success was lower on all treatment plots than on control plots in the southern region and marginally lower on light disturbance plots in the northern region. Our data suggest that only habitats in the southern region acted as sources, and interior disturbances in this region have the potential to create ecological traps at a local scale, but sources when viewed at broader scales. Thus, cerulean warblers would likely benefit from management that strikes a landscape-level balance between emulating natural disturbances in order to attract individuals into areas where current structure is inappropriate, and limiting anthropogenic disturbance in forests that already possess appropriate structural attributes in order to maintain maximum productivity.
Subject(s)
Ecosystem , Songbirds/physiology , Trees/physiology , Animals , Appalachian Region , Conservation of Natural Resources , Female , Male , Models, Biological , Population Density , Population Dynamics , Reproduction , Songbirds/anatomy & histologyABSTRACT
Preening is the principle behavioral defense used by birds to combat ectoparasites. Most birds have a small overhang at the tip of their bills that is used to shear through the tough cuticle of ectoparasitic arthropods, making preening much more efficient. Birds may also scratch with their feet to defend against ectoparasites. This is particularly important for removing ectoparasites on the head, which birds cannot preen. Scratching may be enhanced by the comb-like serrations that are found on the claws of birds in many avian families. We examined the prevalence and intensity of ectoparasites of barn owls (Tyto alba pratincola) in southern Idaho in relation to bill hook length and morphological characteristics of the pectinate claw. The barn owls in our study were infested with 3 species of lice (Phthiraptera: Ischnocera): Colpocephalum turbinatum , Kurodaia subpachygaster, and Strigiphilus aitkeni . Bill hook length was associated with the prevalence of these lice. Owls with longer hooks were more likely to be infested with lice. Conventional wisdom suggests that the bill morphology of raptors has been shaped by selection for efficient foraging; our data suggest that hook morphology may also play a role in ectoparasite defense. The number of teeth on the pectinate claw was also associated with the prevalence of lice. Owls that had claws with more teeth were less likely to be infested with lice, which suggests that larger pectinate claws may offer relatively more protection against ectoparasitic lice. Experiments that manipulate the bill hook and pectinate claw are needed to confirm whether these host characters are involved in ectoparasite defense. Finally, we recovered mammalian ectoparasites from 4 barn owls. We recovered species of mammalian lice (Phthiraptera:Anoplura) and fleas (Siphonaptera) that are commonly found on microtine rodents. The owls probably acquired these parasites from recently eaten prey. This represents 1 of the few documented cases of parasites "straggling" from prey to predator.