Habitat-linked genetic variation supports microgeographic adaptive divergence in an island-endemic bird species.

We investigated the potential mechanisms driving habitat-linked genetic divergence within a bird species endemic to a single 250-km2 island. The island scrub-jay (Aphelocoma insularis) exhibits microgeographic divergence in bill morphology across pine-oak ecotones on Santa Cruz Island, California (USA), similar to adaptive differences described in mainland congeners over much larger geographic scales. To test whether individuals exhibit genetic differentiation related to habitat type and divergence in bill length, we genotyped over 3000 single nucleotide polymorphisms in 123 adult island scrub-jay males from across Santa Cruz Island using restriction site-associated DNA sequencing. Neutral landscape genomic analyses revealed that genome-wide genetic differentiation was primarily related to geographic distance and differences in habitat composition. We also found 168 putatively adaptive loci associated with habitat type using multivariate redundancy analysis while controlling for spatial effects. Finally, two genome-wide association analyses revealed a polygenic basis to variation in bill length with multiple loci detected in or near genes known to affect bill morphology in other birds. Our findings support the hypothesis that divergent selection at microgeographic scales can cause adaptive divergence in the presence of ongoing gene flow.

Hunting alters viral transmission and evolution in a large carnivore.

Hunting can fundamentally alter wildlife population dynamics but the consequences of hunting on pathogen transmission and evolution remain poorly understood. Here, we present a study that leverages a unique landscape-scale quasi-experiment coupled with pathogen-transmission tracing, network simulation and phylodynamics to provide insights into how hunting shapes feline immunodeficiency virus (FIV) dynamics in puma (Puma concolor). We show that removing hunting pressure enhances the role of males in transmission, increases the viral population growth rate and increases the role of evolutionary forces on the pathogen compared to when hunting was reinstated. Changes in transmission observed with the removal of hunting could be linked to short-term social changes while the male puma population increased. These findings are supported through comparison with a region with stable hunting management over the same time period. This study shows that routine wildlife management can have impacts on pathogen transmission and evolution not previously considered.

Host relatedness and landscape connectivity shape pathogen spread in the puma, a large secretive carnivore.

Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood. Here, we combine high resolution host and viral genomic data with landscape variables to examine the context of viral spread in puma (Puma concolor) from two contrasting regions: one bounded by the wildland urban interface (WUI) and one unbounded with minimal anthropogenic development (UB). We found landscape variables and host gene flow explained significant amounts of variation of feline immunodeficiency virus (FIV) spread in the WUI, but not in the unbounded region. The most important predictors of viral spread also differed; host spatial proximity, host relatedness, and mountain ranges played a role in FIV spread in the WUI, whereas roads might have facilitated viral spread in the unbounded region. Our research demonstrates how anthropogenic landscapes can alter pathogen spread, providing a more nuanced understanding of host-pathogen relationships to inform disease ecology in free-ranging species.

Correction: Male principal investigators (almost) don't publish with women in ecology and zoology.

[This corrects the article DOI: 10.1371/journal.pone.0218598.].

Genomic and Fitness Consequences of Genetic Rescue in Wild Populations.

Gene flow is an enigmatic evolutionary force because it can limit adaptation but may also rescue small populations from inbreeding depression [1-3]. Several iconic examples of genetic rescue-increased population growth caused by gene flow [4, 5]-have reversed population declines [6, 7]. However, concerns about outbreeding depression and maladaptive gene flow limit the use of human-mediated gene flow in conservation [8, 9]. Rescue effects of immigration through demographic and/or genetic mechanisms have received theoretical and empirical support, but studies that monitor initial and long-term effects of gene flow on individuals and populations in the wild are lacking. Here, we used individual-based mark-recapture, multigenerational pedigrees, and genomics to test the demographic and evolutionary consequences of manipulating gene flow in two isolated, wild Trinidadian guppy populations. Recipient and source populations originated from environments with different predation, flow, and resource regimes [10]. We documented 10-fold increases in population size following gene flow and found that, on average, hybrids lived longer and reproduced more than residents and immigrants. Despite overall genomic homogenization, alleles potentially associated with local adaptation were not entirely swamped by gene flow. Our results suggest that genetic rescue was caused not just by increasing individual genetic diversity, rather new genomic variation from immigrants combined with alleles from the recipient population resulted in highly fit hybrids and subsequent increases in population size. Contrary to the classic view of maladaptive gene flow, our study reveals conditions under which immigration can produce long-term fitness benefits in small populations without entirely swamping adaptive variation.

Urbanization reduces genetic connectivity in bobcats (Lynx rufus) at both intra- and interpopulation spatial scales.

Urbanization is a major factor driving habitat fragmentation and connectivity loss in wildlife. However, the impacts of urbanization on connectivity can vary among species and even populations due to differences in local landscape characteristics, and our ability to detect these relationships may depend on the spatial scale at which they are measured. Bobcats (Lynx rufus) are relatively sensitive to urbanization and the status of bobcat populations is an important indicator of connectivity in urban coastal southern California. We genotyped 271 bobcats at 13,520 SNP loci to conduct a replicated landscape resistance analysis in five genetically distinct populations. We tested urban and natural factors potentially influencing individual connectivity in each population separately, as well as study-wide. Overall, landscape genomic effects were most frequently detected at the study-wide spatial scale, with urban land cover (measured as impervious surface) having negative effects and topographic roughness having positive effects on gene flow. The negative effect of urban land cover on connectivity was also evident when populations were analyzed separately despite varying substantially in spatial area and the proportion of urban development, confirming a pervasive impact of urbanization largely independent of spatial scale. The effect of urban development was strongest in one population where stream habitat had been lost to development, suggesting that riparian corridors may help mitigate reduced connectivity in urbanizing areas. Our results demonstrate the importance of replicating landscape genetic analyses across populations and considering how landscape genetic effects may vary with spatial scale and local landscape structure.

Urbanization impacts apex predator gene flow but not genetic diversity across an urban-rural divide.

Apex predators are important indicators of intact natural ecosystems. They are also sensitive to urbanization because they require broad home ranges and extensive contiguous habitat to support their prey base. Pumas (Puma concolor) can persist near human developed areas, but urbanization may be detrimental to their movement ecology, population structure, and genetic diversity. To investigate potential effects of urbanization in population connectivity of pumas, we performed a landscape genomics study of 130 pumas on the rural Western Slope and more urbanized Front Range of Colorado, USA. Over 12,000 single nucleotide polymorphisms (SNPs) were genotyped using double-digest, restriction site-associated DNA sequencing (ddRADseq). We investigated patterns of gene flow and genetic diversity, and tested for correlations between key landscape variables and genetic distance to assess the effects of urbanization and other landscape factors on gene flow. Levels of genetic diversity were similar for the Western Slope and Front Range, but effective population sizes were smaller, genetic distances were higher, and there was more admixture in the more urbanized Front Range. Forest cover was strongly positively associated with puma gene flow on the Western Slope, while impervious surfaces restricted gene flow and more open, natural habitats enhanced gene flow on the Front Range. Landscape genomic analyses revealed differences in puma movement and gene flow patterns in rural versus urban settings. Our results highlight the utility of dense, genome-scale markers to document subtle impacts of urbanization on a wide-ranging carnivore living near a large urban center.

Male principal investigators (almost) don't publish with women in ecology and zoology.

Representation of women in science drops substantially at each career stage, from early student to senior investigator. Disparities in opportunities for women to contribute to research metrics, such as distinguished speaker events and authorship, have been reported in many fields in the U.S.A. and Europe. However, whether female representation in scientific contributions differs in other regions, such as Latin America, is not well understood. In this study, in order to determine whether female authorship is influenced by gender or institutional location of the last (senior) author or by subfield within ecology, we gathered author information from 6849 articles in ten ecological and zoological journals that publish research articles either in or out of Latin America. We found that female authorship has risen marginally since 2002 (27 to 31%), and varies among Latin American countries, but not between Latin America and other regions. Last author gender predicted female co-authorship across all journals and regions, as research groups led by women published with over 60% female co-authors whereas those led by men published with less than 20% female co-authors. Our findings suggest that implicit biases and stereotype threats that women face in male-led laboratories could be sources of female withdrawal and leaky pipelines in ecology and zoology. Accordingly, we encourage every PI to self-evaluate their lifetime percentage of female co-authors. Female role models and cultural shifts-especially by male senior authors-are crucial for female retention and unbiased participation in science.

The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations.

The success rate of weed biological control programs is difficult to evaluate and the factors affecting it remain poorly understood. One aspect which is still unclear is whether releases of multiple, genetically distinct populations of a biological control agent increase the likelihood of success, either by independent colonization of different environmental niches or by hybridization that may increase the agent's fitness and adaptive ability. Since hybridization is often invoked to explain the success of unintentionally introduced exotic species, hybridization among biocontrol agents may be similarly important in shaping the effectiveness of biological control programs. In this study, we first evaluated intraspecific hybridization among populations of a weed biological control agent, the ragwort flea beetle, Longitarsus jacobaeae. These insects were introduced as part of a classical biological control program from Italy and Switzerland. We genotyped 204 individuals from 15 field sites collected in northwest Montana, and an additional 52 individuals that served as references for Italian and Swiss populations. Bayesian analysis of population structure assigned seven populations as pure Swiss and one population as pure Italian, while intraspecific hybrid individuals were detected in seven populations at frequencies of 5%-69%. Subsequently, we conducted a 2-year exclusion experiment using six sites with Swiss beetles and three with hybrid beetles to evaluate the impact of biological control. We found that biological control by Swiss beetles and by hybrid beetles is effective, increasing mortality of the target plant, Jacobaea vulgaris, by 42% and 45%, and reducing fecundity of surviving plants by 44% and 72%, respectively. Beetle densities were higher and mortality of larger plants was higher at sites with hybrids present. These results suggest that hybridization of ragwort flea beetles at high-elevation sites may improve biological control of tansy ragwort and that intraspecific hybridization of agents could benefit biological control programs.

A new species of Hyloscirtus (Anura, Hylidae) from the Colombian and Venezuelan slopes of Sierra de Perijá, and the phylogenetic position of Hyloscirtus jahni (Rivero, 1961).

A new species of Hyloscirtus, belonging to the H. bogotensis species Group, is described from the Venezuelan and Colombian slopes of the Sierra de Perijá. The new species can be readily distinguished from its congeners by the combination of the following characters: mental gland present, disc-shaped and small; ulnar, outer, and inner tarsal folds present; calcar tubercle absent; whitish stripes on external border of upper eyelids and supratympanic folds, longitudinally on the mid-dorsum, on supracloacal fold, outer ulnar folds, inner and outer tarsal folds, and also on dorsal internal surface of shanks. We estimate phylogenetic relationships based on mtDNA (spanning fragments of 12S rRNA, tRNA-Val and 16S rRNA), of all Hyloscirtus species available in Genbank, as well as the new species described herein, H. callipeza, H. jahni, and H. platydactylus, all of which have not been previously sequenced. Our molecular data support the hypothesis of the new species as sister species of H. callipeza and indicates that H. jahni does not belong to the H. bogotensis species Group, but rather is sister species of all other Hyloscirtus (sensu Faivovich et al. 2005). Based on this last result we propose a new species group for H. jahni and the synonymy of Colomascirtus in Hyloscirtus. We also provide the first description of the advertisement call of H. callipeza. With the new species described herein, the number of Hyloscirtus species increases to 37.

Extreme streams: species persistence and genomic change in montane insect populations across a flooding gradient.

The ecological and evolutionary consequences of extreme events are poorly understood. Here, we tested predictions about species persistence and population genomic change in aquatic insects in 14 Colorado mountain streams across a hydrological disturbance gradient caused by a one in 500-year rainfall event. Taxa persistence ranged from 39 to 77% across sites and declined with increasing disturbance in relation to species' resistance and resilience traits. For taxa with mobile larvae and terrestrial adult stages present at the time of the flood, average persistence was 84% compared to 25% for immobile taxa that lacked terrestrial adults. For two of six species analysed, genomic diversity (allelic richness) declined after the event. For one species it greatly expanded, suggesting resilience via re-colonisation from upstream populations. Thus, while resistance and resilience traits can explain species persistence to extreme disturbance, population genomic change varies among species, challenging generalisations about evolutionary responses to extreme events at landscape scales.

Systematics of Ecnomiohyla tuberculosa with the description of a new species and comments on the taxonomy of Trachycephalus typhonius (Anura, Hylidae).

Ecnomiohyla tuberculosa is an Amazonian hylid of uncertain phylogenetic position. Herein DNA sequences of mitochondrial and nuclear genes are used to determine its phylogenetic relationships. New sequences and external morphology of Trachycephalus typhonius are also analyzed to assess the status of Ecuadorian and Peruvian populations. The phylogeny shows unequivocally that Ecnomiohyla tuberculosa is nested within the genus Tepuihyla, tribe Lophiohylini. This position was unexpected because the remaining species of Ecnomiohyla belong to the tribe Hylini. To solve the paraphyly of the genus Ecnomiohyla, Ecnomiohyla tuberculosa is transferred to the genus Tepuihyla. Comparisons of DNA sequences, external morphology, and advertisement calls between populations of Ecnomiohyla tuberculosa from Ecuador and Peru indicate that the Peruvian population represents an undescribed species. The new species is described and a species account is provided for Ecnomiohyla tuberculosa. Trachycephalus typhonius is paraphyletic relative to Trachycephalus cunauaru, Trachycephalus hadroceps, and Trachycephalus resinifictrix. The phylogenetic position of populations from western Ecuador indicates that they represent a species separate from Trachycephalus typhoniussensu stricto. We resurrect the name Hyla quadrangulum (Trachycephalus quadrangulumcomb. n.) for those populations. Amazonian populations of "Trachycephalus typhonius" from Ecuador and Peru are genetically and morphologically distinct from Trachycephalus typhoniussensu stricto and are conspecific with the holotype of Hyla macrotis. Therefore, we also resurrect Hyla macrotis, a decision that results in Trachycephalus macrotiscomb. n.

Terraranans of the Lost World: a new species of Pristimantis (Amphibia, Craugastoridae) from Abakapá-tepui in the Chimantá massif, Venezuelan Guayana, and additions to the knowledge of P. muchimuk.

A new frog of the genus Pristimantis is named and described from the summit of Abakapá-tepui in the Chimantd massif, south-eastern Venezuela. The new species is known from two adult specimens and is the second craugastorid species described from this massif. It can be readily distinguished from all congeners inhabiting the highlands of the Guiana Shield by the unique combination of the following characters: dorsal skin shagreen and ventral skin coarsely areolate, tympanum small and ill-defined, vocal slits absent in males, finger I shorter than II, thumbs with two whitish and non-spinous nuptial pads in adult males, fingers and toes with broad lateral fringes, basal webbing between all toes, throat and chest nacreous white in life. Also, based on five specimens of Pristimantis muchimuk recently collected from Churi-tepui, we provide new information on this little known species, including an amended diagnosis, notes on morphology, color variation, advertisement calls, and natural history.

Ancient tepui summits harbor young rather than old lineages of endemic frogs.

The flattop mountains (tepuis) of South America are ancient remnants of the Precambrian Guiana Shield plateau. The tepui summits, isolated by their surrounding cliffs that can be up to 1000 m tall, are thought of as "islands in the sky," harboring relict flora and fauna that underwent vicariant speciation due to plateau fragmentation. High endemicity atop tepui summits support the idea of an ancient "Lost World" biota. However, recent work suggests that dispersal between lowlands and summits has occurred long after tepui formation indicating that tepui summits may not be as isolated from the lowlands as researchers have long suggested. Neither view of the origin of the tepui biota (i.e., ancient vicariance vs. recent dispersal) has strong empirical support owing to a lack of studies. We test diversification hypotheses of the Guiana Shield highlands by estimating divergence times of an endemic group of treefrogs, Tepuihyla. We find that diversification of this group does not support an ancient origin for this taxon; instead, divergence times among the highland species are 2-5 Ma. Our data indicate that most highland speciation occurred during the Pliocene. Thus, this unparalleled landscape known as "The Lost World" is inhabited, in part, not by Early Tertiary relicts but neoendemics.