ABSTRACTIncidental mortality in fisheries is a major driver of population declines for albatrosses and petrels globally. However, accurate identification of species can be difficult due to the poor condition of bycaught birds and/or visual similarities between closely related species. We assessed three genetic markers for their ability to distinguish the 36 albatross and petrel species listed in Annex 1 to the Agreement on the Conservation of Albatrosses and Petrels (ACAP) and in Australia's Threat Abatement Plan (TAP) for the bycatch of seabirds during oceanic longline fishing operations. We generated 275 new sequences, from 29 species, to improve the coverage of reference databases for these listed species. The combined use of the selected Cytochrome b and Control Region markers enabled the identification of 31 of 36 listed seabirds to species level and four to sister species. One petrel species could not be evaluated as no reference sequences were available. We tested these markers on 59 feathers from bycaught seabirds and compared these to onboard visual identification. We successfully assigned all procellariiforms to species (n = 58), whereas only two seabirds were correctly identified to species visually onboard, highlighting the difficulty of visual species assignment and the need for alternative methods. We assessed the utility of our two chosen markers for the assignment of all procellariiform species, with 74% of species with reference sequences identified to species or sister species level. However, a precautionary approach is needed for application beyond our listed species due to unvalidated reference sequences. The approach described here provides a streamlined framework for the molecular identification of seabird bycatch. This approach is recommended for use in fisheries within and outside Australian waters to improve the resolution of bycatch reporting and to corroborate logbook entries, observer reports and audits of images captured by electronic monitoring systems as well as help inform conservation efforts.
A small colony of black-browed albatrosses (Thalassarche melanophris, 21–65 breeding pairs) was discovered in 2003 on Albatross Islet, Tierra del Fuego, Chile. The formation of new breeding sites is important from an ecological and evolutionary perspective. This colony is particularly significant because it is the only one recorded for the species in a land-locked area. As its population dynamics could be shaped by stochastic and other factors affecting small populations, understanding the variables influencing its persistence, such as source of breeders, is crucial. Here, we used genetic markers (mitochondrial control region) to determine the origin of individuals at this new breeding site. Our results show that the new colony is an even mix of birds from Chilean colonies to the south and west (52
Species reintroductions have the potential to cause genetic bottleneck events resulting in increased genetic drift, increased inbreeding, and reduced genetic diversity creating negative fitness consequences for populations. Roosevelt elk ( Cervus canadensis roosevelti Erxleben, 1777) are “at risk” in British Columbia (BC), Canada. Once widespread along the west coast, Roosevelt elk were likely extirpated from the mainland by 1900 and experienced a substantial population bottleneck on Vancouver Island at that time, and again in the 1950s. Reintroduced to the mainland from Vancouver Island in the 1980s, this re-established population became the source for subsequent mainland translocations. To understand the effects of reintroduction strategy on genetic diversity, we analyzed genetic variation in 355 Roosevelt elk from Vancouver Island and mainland BC. Using mitochondrial DNA and 10 microsatellite loci, molecular analyses showed overall reduced genetic diversity relative to other extant elk populations, genetic isolation of the southern Vancouver Island population, and increased genetic drift among reintroduced herds. Four reintroduced populations were found to have increased levels of inbreeding. Results of this study contribute to our knowledge of reintroduction biology and can be used to guide continued conservation and management of at-risk species.
Animals are strongly connected to the environments they live in and may become adapted to local environments. Examining genetic-environment associations of key indicator species, like seabirds, provides greater insights into the forces that drive evolution in marine systems. Here we examined a RADseq dataset of 19,213 SNPs for 99 rhinoceros auklets (Cerorhinca monocerata) from five western Pacific and 10 eastern Pacific breeding colonies. We used partial redundancy analyses to identify candidate adaptive loci and to quantify the effects of environmental variation on population genetic structure. We identified 262 candidate adaptive loci, which accounted for 3.0% of the observed genetic variation among western Pacific and eastern Pacific breeding colonies. Genetic variation was more strongly associated with pH and maximum current velocity, than maximum sea surface temperature. Genetic-environment associations explain genetic differences between western and eastern Pacific populations; however, genetic variation within the western and eastern Pacific Ocean populations appears to follow a pattern of isolation-by-distance. This study represents a first to quantify the relationship between environmental and genetic variation for this widely distributed marine species and provides greater insights into the evolutionary forces that act on marine species.
The southern oceans are home to a large variety of organisms, including many endemic species. High levels of endemism are due in part to non-physical barriers limiting gene flow in marine species. The sooty albatross Phoebetria fusca is an endangered seabird breeding on seven island groups in Atlantic and Indian Oceans. We sequenced the mitochondrial control region (55 birds) and genotyped 10 microsatellite markers (88 birds) to examine the population genetics of sooty albatrosses from Tristan da Cunha and Gough Island (Atlantic Ocean), and Marion Island, Île de la Possession (Crozet) and Amsterdam Island (Indian Ocean), which together support > 99
Population genetic structure is influenced by a combination of contemporary and historical events; however, this structure can be complicated by ongoing gene flow. While it is well known that contemporary hybridization occurs frequently among many closely related species, it often remains uncertain as to which populations are involved in introgression events, and this can be even more difficult to infer when introgression is historical. Here we use restriction-site associated DNA sequencing to look at the level of introgression among four species of songbirds in North America: the black-capped, mountain, boreal, and chestnut-backed chickadee. Samples from both sympatric and allopatric sites across the species' ranges supported limited ongoing mixing among the four species with Bayesian clustering and principal component analyses. In contrast, f4-statistics and admixture graphs revealed extensive historical introgression among geographically structured populations. Almost all historical admixture events were among populations west of the Rocky Mountains, and almost all populations west of the Rocky Mountains, excluding island and coastal populations, showed evidence of historical admixture. The inclusion of all four chickadee species proved crucial in differentiating which species were involved in hybridization events to avoid erroneous conclusions. Taken together, the results suggest a complex pattern of divergence with gene flow.
ABSTRACT For most birds that exhibit delayed dispersal (remaining on the natal territory rather than dispersing to seek a breeding opportunity), siblings appear free to stay or leave the natal area. However, in rare cases, delaying dispersal is determined via conflict among siblings, with the dominant individual remaining on the natal territory. We used radio-tracking to examine brood reduction, and subsequent juvenile survival, of first-year Canada Jays (Perisoreus canadensis) in Algonquin Provincial Park, Ontario, Canada. Soon after juveniles become nutritionally independent, intra-brood struggles lead to one “dominant juvenile” remaining on the natal territory after permanently expelling the subordinate siblings (“ejectees”). Males in above-average condition when nestlings were the most likely to become the dominant juveniles and females did so only when broods were all-female at the time of the expulsion. Dominant juveniles were much more likely to survive their first summer compared to ejectees (survival probabilities = 0.84 and 0.45, respectively), suggesting that ejectees are especially vulnerable to mortality risk in the critical interval between their expulsion from the natal territory and their settlement on a new territory. However, if ejectees lived to autumn, they had only a slightly lower probability of first-winter survival (0.73) than dominant juveniles (0.85). These results suggest that the survival advantage gained by dominant juveniles is greatest during the first summer after hatching, with a much smaller difference over the first winter after ejectees have settled on non-natal territories. Our work provides insight into potential evolutionary and ecological mechanisms driving social dominance hierarchies in wild birds.
Many species-at-risk reach the edge of their range as disjunct and isolated populations. These peripheral populations may harbour unique genetic diversity crucial for future range shifts, or they may lack genetic diversity due to isolation or small population size. As such it is important to assess the genetic diversity and differentiation of these populations. We used 1,838 SNPs to evaluate the differentiation and genetic diversity in six Canadian (peripheral) and eight US (core) populations of wood-poppy (Stylophorum diphyllum), a perennial wildflower that is endangered at the northern limit of its range. We also compared these 14 populations to seeds from two commercial seed providers to determine if commercial sources are introgressing into wild populations. We found strong differentiation between core and peripheral populations, low levels of gene flow among both core and peripheral populations, and low to moderate levels of genetic diversity across the range with a decrease in heterozygosity in peripheral populations. We also noted that the commercial populations were genetically distinct from all natural sampled populations, with no evidence of introgression between commercial seeds and either Canadian or US populations. Our study indicates that peripheral and core populations form unique conservation units and therefore the conservation and recovery of the wood-poppy in Canada is necessary to conserve the full range of genetic diversity within the species.
Differences in life history can cause co-distributed species to display discordant population genetic patterns. In high-latitude animals, evolutionary processes may be especially influenced by long-distance seasonal migration, a widespread adaptation to seasonality. Although migratory movements are intuitively linked to dispersal, their evolutionary genetic consequences remain poorly understood. Using ~1700 genomes from 35 co-distributed boreal-breeding bird species, we reveal that most long-distance migrants exhibit spatial genetic structure, revealing evolutionary effects of philopatry rather than dispersal. We further demonstrate that migration distance and genetic diversity are strongly positively correlated in our study species. This striking relationship suggests that the adaptive seasonal shifts in biogeography that long-distance migratory species undergo each year lends them enhanced population stability that preserves genetic diversity relative to shorter-distance migrants that winter at higher latitudes. Our results suggest that the major impact of long-distance seasonal migration on population genetic evolution occurs through promotion of demographic stability, rather than facilitation of dispersal. ### Competing Interest Statement The authors have declared no competing interest.
Abstract Understanding how both contemporary and historical physical barriers influence gene flow is key to reconstructing evolutionary histories and can allow us to predict species' resilience to changing environmental conditions. During the last glacial maximum (LGM), many high latitude North American bird species were forced into glacial refugia, including mountain bluebirds (Silia currucoides). Within their current breeding range, mountain bluebirds still experience a wide variety of environmental conditions and barriers that may disrupt gene flow and isolate populations. Using single nucleotide polymorphisms (SNPs) obtained through restriction site‐associated DNA sequencing, we detected at least four genetically distinct mountain bluebird populations. Based on this structure, we determined that isolation‐by‐distance, the northern Rocky Mountains, and discontinuous habitat are responsible for the low connectivity and the overall history of each population going back to the last glacial maximum. Finally, we identified five candidate genes under balancing selection and three loci under diversifying selection. This study provides the first look at connectivity and gene flow across the range of these high‐altitude and high latitude songbirds.
Anthropogenic climate change has a large impact on wildlife populations and the scale of the impacts has been increasing. In this study, we utilised 3dRAD sequence data to investigate genetic divergence and identify the environmental drivers of genetic differentiation between 12 populations of mountain chickadees, family Paridae, sampled across North America. To examine patterns of genetic variation across the range, we conducted a discriminant analysis of principal components (DAPC), admixture analysis, and calculated pairwise Fst values. The DAPC revealed four clusters: southern California, eastern Rocky Mountains, northwestern Rocky Mountains, and Oregon/northern California. We then used BayeScEnv to highlight significant outlier SNPs associated with the five environmental variables. We identified over 150 genes linked to outlier SNPs associated with more than 15 pathways, including stress response and circadian rhythm. We also found a strong signal of isolation by distance and local temperature was highly correlated with genetic distance. Maxent simulations showed a northward range shift over the next 50 years and a decrease in suitable habitat, highlighting the need for immediate conservation action.
Examining the frequency and distribution of hybrids across contact zones provide insights into the factors mediating hybridization. In this study, we examined the effect of habitat and climate on hybridization patterns for three phenotypically, genetically, and ecologically distinct groups of the Canada jay (Perisoreus canadensis) in a secondary contact zone in western North America. Additionally, we tested whether the frequency of hybridization involving the three groups (referred to as Boreal, Pacific and Rocky Mountain morphotypes) is similar across the hybrid zones or whether some pairs have hybridized more frequently than others. We reanalyzed microsatellite, mtDNA and plumage data, and new microsatellite and plumage data for 526 individuals to identify putative genetic and phenotypic hybrids. The genetically and phenotypically distinct groups are associated with different habitats and occupy distinct climate niches across the contact zone. Most putative genetic hybrids (86%) had Rocky Mountain ancestry. Hybrids were observed most commonly in intermediate climate niches and in habitats where Engelmann spruce (Picea engelmannii) overlaps broadly with boreal and subalpine tree species. Our finding that hybrids occupy intermediate climate niches relative to parental morphotypes matches patterns for other plant and animal species found in this region. This study demonstrates how habitat and climate influence hybridization patterns in areas of secondary contact and adds to the growing body of research on tri-species hybrid zones.
Tufted Puffins (Fratercula cirrhata) are experiencing population declines in some parts of their distribution, making this a species of increased conservation interest. Genetic data will help to identify Tufted Puffin populations of conservation importance and provide an important tool for developing conservation management plans. This species is broadly distributed across the North Pacific Ocean but little is known about the extent of genetic variation and differentiation across their range. In this study, we examine mitochondrial DNA (mtDNA), 8 microsatellite loci and 1,260 single nucleotide polymorphisms (SNPs) to determine the extent of gene flow among 7 breeding colonies (Oregon to the western Aleutians) in the North American breeding range of the species and identify potential barriers to dispersal. Our results show that most breeding colonies form a single genetic cluster, and mtDNA data show substantial historical gene flow among populations. For the microsatellite dataset, all F-ST comparisons that include St. Lazaria, in southeast Alaska, except Oregon, which had a small sample size, were significant as were comparisons between Triangle Island and the two westernmost sampling sites of Buldir and Aiktak. For the SNP dataset, F-ST comparisons were low and nonsignificant, further suggesting that breeding colonies form a single panmictic population. Individuals were more closely related to individuals from the same colony, and we found a weak relationship between genetic and geographic distance. This suggests that dispersal among colonies is high, likely facilitated by an overlap in wintering ranges among colonies. The high connectivity among breeding colonies indicates that Tufted Puffins form a single conservation unit, although future genetic studies should incorporate a whole genome sequencing approach to assessing how functional genetic diversity varies across their distribution. Lay Summary & BULL; Tufted Puffins (Fratercula cirrhata) are experiencing population declines in some parts of their distribution, making this a species of increased conservation interest. & BULL; Here we use 3 different types of genetic markers (mtDNA, microsatellites, and SNPs) to examine population genetic structure among 7 breeding colonies (Oregon to the western Aleutians) in the North American breeding range of the species. & BULL; We examined population genetic structure to determine whether Tufted Puffin populations form single or multiple conservation units. & BULL; All 3 types of markers showed a similar pattern and indicate that North American breeding colonies form a single genetic cluster. & BULL; Our results suggest that dispersal among colonies is high, likely facilitated by an overlap in wintering ranges among colonies. & BULL; The high connectivity among breeding colonies indicates that Tufted Puffins form a single conservation unit, although future genetic studies should include samples from Asia to assess population genetic structure across their whole distribution.
Advances in technology and software have provided higher resolution of genetic data. Re-analysis of genetic data from the endangered Antipodean Albatross using STRUCTURE shows that samples from the two main breeding populations on Antipodes and Adams Islands can be assigned correctly to each population using a set of nine microsatellite markers. The new analyses allow for assignment of bycatch birds killed off the east coast of New Zealand with high accuracy and show all of them originated from Antipodes Island. This highlights not only the importance of using genetic markers to inform conservation and management of endangered species but also the important advances in bioinformatics and the value of existing datasets.
Identifying population genetic structure is important for the development of species-specific management plans. Investigating the population genetics of cryptic species is even more critical. Here we focus on two cryptic duckweed species easily mistaken for one another, Lemna minor L. and L. turionifera Landolt, which have overlapping ranges in our study region of Alberta, Canada, and elsewhere. We used genotyping-by-sequencing to determine the population genetic structure of both duckweed species. A total of 192 samples was sequenced. After filtering, 16,007 single nucleotide polymorphisms were used to examine patterns of genetic diversity between and within L. minor and L. turionifera. The two species showed clear differentiation. When examining L. minor singly, we discovered at least three genetically distinct populations among the 30 samples from eight sites, even though these were from a small geographic area. In contrast, when examining L. turionifera singly, we found no evidence of genetically distinct populations among 67 samples from 43 sites. We also examined the relationship between surface water quality variables and the distribution of the two Lemna species. The sites containing L. turionifera had a wider range of water chemistry variables suggesting they are more tolerant of different environmental conditions. In contrast, each of the three genetically distinct L. minor groups had different water chemistry profiles. Large differences between L. minor and L. turionifera in their regional distributions and degrees of genetic differentiation highlight the importance of documentation and careful monitoring of Lemna species within Alberta, and in other regions where they co-occur.
Following postglacial expansion, secondary contact can occur between genetically distinct lineages. These genetic lineages may be associated with specific habitat or environmental variables and therefore, their distributions in secondary contact could reflect such conditions within these areas. Here we used mtDNA, microsatellite, and morphological data to study three genetically distinct groups of warbling vireo (Vireo gilvus) and investigate the role that elevation and habitat play in their distributions. We studied two main contact zones and within each contact zone, we examined two separate transects. Across the Great Plains contact zone, we found that hybridization between eastern and western groups occurs along a habitat and elevational gradient, whereas hybridization across the Rocky Mountain contact zone was not as closely associated with habitat or elevation. Hybrids in the Great Plains contact zone were more common in transitional areas between deciduous and mixed-wood forests, and at lower elevations (<1000 m). Hybridization patterns were similar along both Great Plains transects indicating that habitat and elevation play a role in hybridization between distinct eastern and western genetic groups. The observed patterns suggest adaptation to different habitats, perhaps originating during isolation in multiple Pleistocene refugia, is facilitating hybridization in areas where habitat types overlap.
Abstract Both abiotic and biotic drivers influence species distributions. Abiotic drivers such as climate have received considerable attention, even though biotic drivers such as hybridization often interact with abiotic drivers. We sought to explore the (1) costs of co‐occurrence for ecologically similar species that hybridize and (2) associations between ecological factors and condition to understand how abiotic and biotic factors influence species distributions. For two closely related and ecologically similar songbirds, black‐capped and mountain chickadees, we characterized body condition, as a proxy for fitness, using a 1358‐individual range‐wide dataset. We compared body condition in sympatry and allopatry with several abiotic and biotic factors using species‐specific generalized linear mixed models. We generated genomic data for a subset of 217 individuals to determine the extent of hybridization‐driven admixture in our dataset. Within this data subset, we found that ~11% of the chickadees had hybrid ancestry, and all hybrid individuals had typical black‐capped chickadee plumage. In the full dataset, we found that birds of both species, independent of demographic and abiotic factors, had significantly lower body condition when occurring in sympatry than birds in allopatry. This could be driven by either the inclusion of cryptic, likely poor condition, hybrids in our full dataset, competitive interactions in sympatry, or range edge effects. We are currently unable to discriminate between these mechanisms. Our findings have implications for mountain chickadees in particular, which will encounter more black‐capped chickadees as black‐capped chickadee ranges shift upslope and could lead to local declines in mountain chickadee populations.
Human habitat disturbances can promote hybridization between closely related, but typically reproductively isolated, species. We explored whether human habitat disturbances are related to hybridization between two closely related songbirds, black-capped and mountain chickadees, using both genomic and citizen science data sets. First, we genotyped 409 individuals from across both species' ranges using reduced-representation genome sequencing and compared measures of genetic admixture to a composite measure of human landscape disturbance. Then, using eBird observations, we compared human landscape disturbance values for sites where phenotypically diagnosed hybrids were observed to locations where either parental species was observed to determine whether hybrid chickadees are reported in more disturbed areas. We found that hybridization between black-capped and mountain chickadees positively correlates with human habitat disturbances. From genomic data, we found that (1) hybrid index (HI) significantly increased with habitat disturbance, (2) more hybrids were sampled in disturbed habitats, (3) mean HIs were higher in disturbed habitats versus wild habitats, and (4) hybrids were detected in habitats with significantly higher disturbance values than parentals. Using eBird data, we found that both hybrid and black-capped chickadees were significantly more disturbance-associated than mountain chickadees. Surprisingly, we found that nearly every black-capped chickadee we sampled contained some proportion of hybrid ancestry, while we detected very few mountain chickadee backcrosses. Our results highlight that hybridization between black-capped and mountain chickadees is widespread, but initial hybridization is rare (few F1s were detected). We conclude that human habitat disturbances can erode pre-zygotic reproductive barriers between chickadees and that post-zygotic isolation is incomplete. Understanding what becomes of recently hybridizing species following large-scale habitat disturbances is a new, but pressing, consideration for successfully preserving genetic biodiversity in a rapidly changing world.