Allele frequency dynamics under sex-biased demography and sex-specific inheritance in a pedigreed jay population.

Sex-biased demography, including sex-biased survival or migration, can alter allele frequency changes across the genome. In particular, we can expect different patterns of genetic variation on autosomes and sex chromosomes due to sex-specific differences in life histories, as well as differences in effective population size, transmission modes, and the strength and mode of selection. Here, we demonstrate the role that sex differences in life history played in shaping short-term evolutionary dynamics across the genome. We used a 25-year pedigree and genomic dataset from a long-studied population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of sex-biased demography and inheritance in shaping genome-wide allele frequency trajectories. We used gene dropping simulations to estimate individual genetic contributions to future generations and to model drift and immigration on the known pedigree. We quantified differential expected genetic contributions of males and females over time, showing the impact of sex-biased dispersal in a monogamous system. Due to female-biased dispersal, more autosomal variation is introduced by female immigrants. However, due to male-biased transmission, more Z variation is introduced by male immigrants. Finally, we partitioned the proportion of variance in allele frequency change through time due to male and female contributions. Overall, most allele frequency change is due to variance in survival and births. Males and females make similar contributions to autosomal allele frequency change, but males make higher contributions to allele frequency change on the Z chromosome. Our work shows the importance of understanding sex-specific demographic processes in characterizing genome-wide allele frequency change in wild populations.

Impacts of increasing isolation and environmental variation on Florida Scrub-Jay demography.

Isolation caused by anthropogenic habitat fragmentation can destabilize populations. Populations relying on the inflow of immigrants can face reduced fitness due to inbreeding depression as fewer new individuals arrive. Empirical studies of the demographic consequences of isolation are critical to understand how populations persist through changing conditions. We used a 34-year demographic and environmental dataset from a population of cooperatively-breeding Florida Scrub-Jays ( Aphelocoma coerulescens ) to create mechanistic models linking environmental and demographic factors to population growth rates. We found that the population has not declined despite both declining immigration and increasing inbreeding, owing to a coinciding response in breeder survival. We find evidence of density-dependent immigration, breeder survival, and fecundity, indicating that interactions between vital rates and local density play a role in buffering the population against change. Our study elucidates the impacts of isolation on demography and how long-term stability is maintained via demographic responses.

Correction: Batch-produced, GIS-informed range maps for birds based on provenanced, crowd-sourced data inform conservation assessments.

[This corrects the article DOI: 10.1371/journal.pone.0259299.].

The structure and organisation of an Amazonian bird community remains little changed after nearly four decades in Manu National Park.

Documenting patterns of spatiotemporal change in hyper-diverse communities remains a challenge for tropical ecology yet is increasingly urgent as some long-term studies have shown major declines in bird communities in undisturbed sites. In 1982, Terborgh et al. quantified the structure and organisation of the bird community in a 97-ha. plot in southeastern Peru. We revisited the same plot in 2018 using the same methodologies as the original study to evaluate community-wide changes. Contrary to longitudinal studies of other neotropical bird communities (Tiputini, Manaus, and Panama), we found little change in community structure and organisation, with increases in 5, decreases in 2 and no change in 7 foraging guilds. This apparent stability suggests that large forest reserves such as the Manu National Park, possibly due to regional topographical influences on precipitation, still provide the conditions for establishing refugia from at least some of the effects of global change on bird communities.

Dynamics of reduced genetic diversity in increasingly fragmented populations of Florida scrub jays,Aphelocoma coerulescens.

Understanding the genomic consequences of population decline is important for predicting species' vulnerability to intensifying global change. Empirical information about genomic changes in populations in the early stages of decline, especially for those still experiencing immigration, remains scarce. We used 7834 autosomal SNPs and demographic data for 288 Florida scrub jays (Aphelocoma coerulescens; FSJ) sampled in 2000 and 2008 to compare levels of genetic diversity, inbreeding, relatedness, and lengths of runs of homozygosity (ROH) between two subpopulations within dispersal distance of one another but have experienced contrasting demographic trajectories. At Archbold Biological Station (ABS), the FSJ population has been stable because of consistent habitat protection and management, while at nearby Placid Lakes Estates (PLE), the population declined precipitously due to suburban development. By the onset of our sampling in 2000, birds in PLE were already less heterozygous, more inbred, and on average more related than birds in ABS. No significant changes occurred in heterozygosity or inbreeding across the 8-year sampling interval, but average relatedness among individuals decreased in PLE, thus by 2008 average relatedness did not differ between sites. PLE harbored a similar proportion of short ROH but a greater proportion of long ROH than ABS, suggesting one continuous population of shared demographic history in the past, which is now experiencing more recent inbreeding. These results broadly uphold the predictions of simple population genetic models based on inferred effective population sizes and rates of immigration. Our study highlights how, in just a few generations, formerly continuous populations can diverge in heterozygosity and levels of inbreeding with severe local population decline despite ongoing gene flow.

Staging to join non-kin groups in a classical cooperative breeder, the Florida scrub-jay.

Why unrelated members form groups in animal societies remains a pertinent topic in evolutionary biology because benefits for group members often are not obvious. We studied subordinates that disperse to join unrelated social groups in the Florida scrub-jay Aphelocoma coerulescens, a cooperative breeding species mainly composed of kin-based groups. We evaluated potential adaptive benefits of dispersing to become an unrelated helper (staging) versus remaining home and dispersing only to pair and breed (direct dispersal) to understand why non-kin-based groups form. Using 35 years of demographic data, we quantified life-history aspects of staging individuals and tested associations between social and ecological factors on the natal and staging territories. We compared fitness outcomes between dispersal strategies by analysing survival, breeding recruitment and direct reproductive output. We tested for sexual asymmetry potentially driven by differences in territory acquisition patterns and female-biased dispersal for this species. Of birds that reached 1 year, 28% staged at a non-natal territory before breeding or disappearing. Staging dispersers departed at younger ages and moved greater distances than direct dispersers. When looking at proximate factors on the natal territory associated with staging, males left groups with many same-sex helpers, while females often left when their father disappeared. For both sexes, staging individuals more likely came from high-quality territories and joined groups with fewer same-sex helpers than in their natal group. While staging and direct dispersers did not differ in survival or likelihood of becoming a breeder, staging males became breeders later and had lower lifetime reproductive success than direct dispersers. In Florida scrub-jays, staging appears to be an alternative strategy for female helpers, but a best-of-a-bad-situation for males. This sexual asymmetry is consistent with males having more options than females to achieve higher reproductive success by breeding near home. Trade-offs in cost-benefits of departing the natal territory and joining unrelated groups as a helper seem to best explain alternative dispersal patterns, with optimal social queues primarily driving the benefits. This research highlights plasticity in dispersal behaviour in response to social and environmental conditions and offers a new perspective in our understanding of non-kin-based social groups.

Batch-produced, GIS-informed range maps for birds based on provenanced, crowd-sourced data inform conservation assessments.

Accurate maps of species ranges are essential to inform conservation, but time-consuming to produce and update. Given the pace of change of knowledge about species distributions and shifts in ranges under climate change and land use, a need exists for timely mapping approaches that enable batch processing employing widely available data. We develop a systematic approach of batch-processing range maps and derived Area of Habitat maps for terrestrial bird species with published ranges below 125,000 km2 in Central and South America. (Area of Habitat is the habitat available to a species within its range.) We combine existing range maps with the rapidly expanding crowd-sourced eBird data of presences and absences from frequently surveyed locations, plus readily accessible, high resolution satellite data on forest cover and elevation to map the Area of Habitat available to each species. Users can interrogate the maps produced to see details of the observations that contributed to the ranges. Previous estimates of Areas of Habitat were constrained within the published ranges and thus were, by definition, smaller-typically about 30%. This reflects how little habitat within suitable elevation ranges exists within the published ranges. Our results show that on average, Areas of Habitat are 12% larger than published ranges, reflecting the often-considerable extent that eBird records expand the known distributions of species. Interestingly, there are substantial differences between threatened and non-threatened species. Some 40% of Critically Endangered, 43% of Endangered, and 55% of Vulnerable species have Areas of Habitat larger than their published ranges, compared with 31% for Near Threatened and Least Concern species. The important finding for conservation is that threatened species are generally more widespread than previously estimated.

Fire history and weather interact to determine extent and synchrony of mast-seeding in rhizomatous scrub oaks of Florida.

In disturbance-prone ecosystems, fitness consequences of plant reproductive strategies are often determined by the relative timing of seed production and disturbance events, but the role of disturbances as proximate drivers of seed production has been overlooked. We use long-term data on seed production in Quercus chapmanii, Q. geminata and Q. inopina, rhizomatous oaks found in south central Florida's oak scrub, to investigate the role of fire history and its interaction with weather in shaping acorn production and its synchrony. Acorn production increased with the time since last fire, combined with additive or interactive effects of spring precipitation (+) or drought (-). Furthermore, multiple matrix regression models revealed that ramet pairs with shared fire history were more synchronous in seed production than ones that burned in different years. Long-term trends suggest that increasingly drier spring weather, in interaction with fire frequency, may drive a decline of seed production. Such declines could affect the community of acorn-reliant vertebrates in the Florida scrub, including endangered Florida scrub-jays (Aphelocoma coerulescens). These results illustrate that fire can function as a proximate driver of seed production in mast-seeding species, highlighting the increasingly recognized importance of interactions among reproductive strategies and disturbance regimes in structuring plant populations and communities. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Allele frequency dynamics in a pedigreed natural population.

A central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes-variation in individual survival, reproductive success, and movement-are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

Climate change causes upslope shifts and mountaintop extirpations in a tropical bird community.

Montane species worldwide are shifting upslope in response to recent temperature increases. These upslope shifts are predicted to lead to mountaintop extinctions of species that live only near mountain summits, but empirical examples of populations that have disappeared are sparse. We show that recent warming constitutes an "escalator to extinction" for birds on a remote Peruvian mountain-high-elevation species have declined in both range size and abundance, and several previously common mountaintop residents have disappeared from the local community. Our findings support projections that warming will likely drive widespread extirpations and extinctions of high-elevation taxa in the tropical Andes. Such climate change-driven mountaintop extirpations may be more likely in the tropics, where temperature seems to exert a stronger control on species' range limits than in the temperate zone. In contrast, we show that lowland bird species at our study site are expanding in range size as they shift their upper limits upslope and may thus benefit from climate change.

Deconstructing isolation-by-distance: The genomic consequences of limited dispersal.

Geographically limited dispersal can shape genetic population structure and result in a correlation between genetic and geographic distance, commonly called isolation-by-distance. Despite the prevalence of isolation-by-distance in nature, to date few studies have empirically demonstrated the processes that generate this pattern, largely because few populations have direct measures of individual dispersal and pedigree information. Intensive, long-term demographic studies and exhaustive genomic surveys in the Florida Scrub-Jay (Aphelocoma coerulescens) provide an excellent opportunity to investigate the influence of dispersal on genetic structure. Here, we used a panel of genome-wide SNPs and extensive pedigree information to explore the role of limited dispersal in shaping patterns of isolation-by-distance in both sexes, and at an exceedingly fine spatial scale (within ~10 km). Isolation-by-distance patterns were stronger in male-male and male-female comparisons than in female-female comparisons, consistent with observed differences in dispersal propensity between the sexes. Using the pedigree, we demonstrated how various genealogical relationships contribute to fine-scale isolation-by-distance. Simulations using field-observed distributions of male and female natal dispersal distances showed good agreement with the distribution of geographic distances between breeding individuals of different pedigree relationship classes. Furthermore, we built coalescent simulations parameterized by the observed dispersal curve, population density, and immigration rate, and showed how incorporating these extensions to Malécot's theory of isolation-by-distance allows us to accurately reconstruct observed sex-specific isolation-by-distance patterns in autosomal and Z-linked SNPs. Therefore, patterns of fine-scale isolation-by-distance in the Florida Scrub-Jay can be well understood as a result of limited dispersal over contemporary timescales.

Dynamic conservation for migratory species.

In an era of unprecedented and rapid global change, dynamic conservation strategies that tailor the delivery of habitat to when and where it is most needed can be critical for the persistence of species, especially those with diverse and dispersed habitat requirements. We demonstrate the effectiveness of such a strategy for migratory waterbirds. We analyzed citizen science and satellite data to develop predictive models of bird populations and the availability of wetlands, which we used to determine temporal and spatial gaps in habitat during a vital stage of the annual migration. We then filled those gaps using a reverse auction marketplace to incent qualifying landowners to create temporary wetlands on their properties. This approach is a cost-effective way of adaptively meeting habitat needs for migratory species, optimizes conservation outcomes relative to investment, and can be applied broadly to other conservation challenges.

Genomic Consequences of Population Decline in the Endangered Florida Scrub-Jay.

Understanding the population genetic consequences of declining population size is important for conserving the many species worldwide facing severe decline [1]. Thorough empirical studies on the impacts of population reduction at a genome-wide scale in the wild are scarce because they demand huge field and laboratory investments [1, 2]. Previous studies have demonstrated the importance of gene flow in introducing genetic variation to small populations [3], but few have documented both genetic and fitness consequences of decreased immigration through time in a natural population [4-6]. Here we assess temporal variation in gene flow, inbreeding, and fitness using longitudinal genomic, demographic, and phenotypic data from a long-studied population of federally Threatened Florida scrub-jays (Aphelocoma coerulescens). We exhaustively sampled and genotyped the study population over two decades, providing one of the most detailed longitudinal investigations of genetics in a wild animal population to date. Immigrants were less heterozygous than residents but still introduced genetic variation into our study population. Owing to regional population declines, immigration into the study population declined from 1995-2013, resulting in increased levels of inbreeding and reduced fitness via inbreeding depression, even as the population remained demographically stable. Our results show that, contrary to conventional wisdom, small peripheral populations that already have undergone a genetic bottleneck may play a vital role in preserving genetic diversity of larger and seemingly stable populations. These findings underscore the importance of investing in the persistence of small populations and maintaining population connectivity in conservation of fragmented species.

Archiving Primary Data: Solutions for Long-Term Studies.

The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.

Mind the gap: genetic distance increases with habitat gap size in Florida scrub jays.

Habitat gap size has been negatively linked to movement probability in several species occupying fragmented landscapes. How these effects on movement behaviour in turn affect the genetic structure of fragmented populations at local scales is less well known. We tested, and confirmed, the hypothesis that genetic differentiation among adjacent populations of Florida scrub jays--an endangered bird species with poor dispersal abilities and a high degree of habitat specialization--increases with the width of habitat gaps separating them. This relationship was not an artefact of simple isolation-by-distance, as genetic distance was not correlated with the Euclidean distance between geographical centroids of the adjacent populations. Our results suggest that gap size affects movement behaviour even at remarkably local spatial scales, producing direct consequences on the genetic structure of fragmented populations. This finding shows that conserving genetic continuity for specialist species within fragmented habitat requires maintenance or restoration of preserve networks in which habitat gaps do not exceed a species-specific threshold distance.

Effects of habitat fragmentation on effective dispersal of Florida scrub-jays.

Studies comparing dispersal in fragmented versus unfragmented landscapes show that habitat fragmentation alters the dispersal behavior of many species. We used two complementary approaches to explore Florida Scrub-Jay (Aphelocoma coerulescens) dispersal in relation to landscape fragmentation. First, we compared dispersal distances of color-marked individuals in intensively monitored continuous and fragmented landscapes. Second, we estimated effective dispersal relative to the degree of fragmentation (as inferred from two landscape indexes: proportion of study site covered with Florida Scrub-Jay habitat and mean distance to nearest habitat patch within each study site) by comparing genetic isolation-by-distance regressions among 13 study sites having a range of landscape structures. Among color-banded individuals, dispersal distances were greater in fragmented versus continuous landscapes, a result consistent with other studies. Nevertheless, genetic analyses revealed that effective dispersal decreases as the proportion of habitat in the landscape decreases. These results suggest that although individual Florida Scrub-Jays may disperse farther as fragmentation increases, those that do so are less successful as breeders than those that disperse short distances. Our study highlights the importance of combining observational data with genetic inferences when evaluating the complex biological and life-history implications of dispersal.

Consequences of heterogeneity in survival probability in a population of Florida scrub-jays.

1. Using data on breeding birds from a 35-year study of Florida scrub-jays Aphelocoma coerulescens (Bosc 1795), we show that survival probabilities are structured by age, birth cohort, and maternal family, but not by sex. Using both accelerated failure time (AFT) and Cox proportional hazard models, the data are best described by models incorporating variation among birth cohorts and greater mortality hazard with increasing age. AFT models using Weibull distributions with the shape parameter > 1 were always the best-fitting models. 2. Shared frailty models allowing for family structure greatly reduce model deviance. The best-fitting models included a term for frailty shared by maternal families. 3. To ask how long a data set must be to reach qualitatively the same conclusions, we repeated the analyses for all possible truncated data sets of 2 years in length or greater. Length of the data set affects the parameter estimates, but not the qualitative conclusions. In all but three of 337 truncated data sets the best-fitting models pointed to same conclusions as the full data set. Shared frailty models appear to be quite robust. 4. The data are not adequate for testing hypotheses as to whether variation in frailty is heritable. 5. Substantial structured heterogeneity for survival exists in this population. Such structured heterogeneity has been shown to have substantial effects in reducing demographic stochasticity.

Ivory-billed woodpecker (Campephilus principalis) persists in continental North America.

The ivory-billed woodpecker (Campephilus principalis), long suspected to be extinct, has been rediscovered in the Big Woods region of eastern Arkansas. Visual encounters during 2004 and 2005, and analysis of a video clip from April 2004, confirm the existence of at least one male. Acoustic signatures consistent with Campephilus display drums also have been heard from the region. Extensive efforts to find birds away from the primary encounter site remain unsuccessful, but potential habitat for a thinly distributed source population is vast (over 220,000 hectares).