Population connectivity buffers genetic diversity loss in a seabird (original) (raw)
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Molecular Ecology, 2001
Geographical variation in two related seabird species, the razorbill ( Alca torda ) and common guillemot ( Uria aalge ), was investigated using sequence analysis of mitochondrial DNA (mtDNA) control regions. We determined the nucleotide sequence of the variable 5 ′ segment of the control region in razorbills and common guillemots from breeding colonies across the Atlantic Ocean. The ecology and life history characteristics of razorbill and common guillemot are in many respects similar. They are both considered highly philopatric and have largely overlapping distributions in temperate and subarctic regions of the North Atlantic, yet the species were found to differ widely in the extent and spatial distribution of mtDNA variation. Moreover, the differences in genetic differentiation and diversity were in the opposite direction to that expected from a consideration of traditional classifications and current population sizes. Indices of genetic diversity were highest in razorbill and varied among colonies, as did genotype frequencies, suggestive of restrictions to gene flow. The distribution of genetic variation suggests that razorbills originated from a refugial population in the south-western Atlantic Ocean through sequential founder events and subsequent expansion in the east and north. In common guillemots, genetic diversity was low and there was a lack of geographical structure, consistent with a recent population bottleneck, expansion and gene flow. We suggest that the reduced level of genetic diversity and differentiation in the common guillemot is caused by an inherent propensity for repeated population bottlenecks and concomitantly unstable population structure related to their specialized feeding ecology.
Biodiversity and Conservation, 2020
The largest anthropogenic extinction events during the Holocene occurred on Pacific islands, where thousands of bird populations were lost. Although ancient DNA approaches have become widely used to monitor the genetic variability of species through time, few studies have been conducted to identify the potential cryptic loss of genetic and species diversity within Pacific seabird species. Here we used heterochronous sampling of mitochondrial DNA (Cytochrome b) in the genus Pterodroma from Norfolk Island to quantify potential loss of genetic and species diversity. We particularly focused on the providence petrel P. solandri whose main breeding colony (* 1,000,000 breeding pairs) became extirpated from Norfolk Island following European settlement circa 1800. We sampled subfossil bones consistent with Pterodroma spp. from Norfolk Island, and performed genetic comparisons with other populations of P. solandri and congeneric species. The majority of subfossil Norfolk Island individuals exhibited the most common mitochondrial haplotype from Lord Howe Island P. solandri, suggesting no appreciable loss of genetic variation as a consequence of the Norfolk Island extirpation. Our findings provide an example where a large seabird population was rapidly extirpated by humans without loss of species-level genetic diversity, probably as a consequence of high connectivity with other populations. However, past connectivity was insufficient to prevent the extirpation itself, which has conservation implications for predicting the resilience of threatened seabirds. In contrast, ancient DNA analyses of smaller Pterodroma bones from Norfolk Island indicate the loss of a second species, potentially P. pycrofti, P. brevipes or another closely related, possibly undescribed taxon, from the Tasman Sea. Keywords Ancient DNA Á High-throughput DNA sequencing Á Seabird Á Petrels Á Population genetics Á Phylogenetics Á Phylogeography Á Pterodroma Á Tasman sea Communicated by Anurag chaurasia.
Quantifying population genetic structure is fundamental to testing hypotheses regarding gene flow, population divergence and dynamics across large spatial scales. In species with highly mobile life-history stages, where it is unclear whether such movements translate into effective dispersal among discrete philopatric breeding populations, this approach can be particularly effective. We used seven nuclear microsatellite loci and mitochondrial DNA (ND2) markers to quantify population genetic structure and variation across 20 populations (447 individuals) of one such species, the European Shag, spanning a large geographical range. Despite high breeding philopatry, rare cross-sea movements and recognized subspecies, population genetic structure was weak across both microsatellites and mitochondrial markers. Furthermore, although isolation-by-distance was detected, microsatellite variation provided no evidence that open sea formed a complete barrier to effective dispersal. These data suggest that occasional long-distance, cross-sea movements translate into gene flow across a large spatial scale. Historical factors may also have shaped contemporary genetic structure: cluster analyses of microsatellite data identified three groups, comprising colonies at southern, mid- and northern latitudes, and similar structure was observed at mitochondrial loci. Only one private mitochondrial haplotype was found among subspecies, suggesting that this current taxonomic subdivision may not be mirrored by genetic isolation.
Historical Demographic Processes Dominate Genetic Variation in Ancient Atlantic Cod Mitogenomes
Frontiers in Ecology and Evolution 9, 2021
Ancient DNA (aDNA) approaches have been successfully used to infer the long-term impacts of climate change, domestication, and human exploitation in a range of terrestrial species. Nonetheless, studies investigating such impacts using aDNA in marine species are rare. Atlantic cod ( Gadus morhua ), is an economically important species that has experienced dramatic census population declines during the last century. Here, we investigated 48 ancient mitogenomes from historical specimens obtained from a range of archeological excavations in northern Europe dated up to 6,500 BCE. We compare these mitogenomes to those of 496 modern conspecifics sampled across the North Atlantic Ocean and adjacent seas. Our results confirm earlier observations of high levels of mitogenomic variation and a lack of mutation-drift equilibrium—suggestive of population expansion. Furthermore, our temporal comparison yields no evidence of measurable mitogenomic changes through time. Instead, our results indicate that mitogenomic variation in Atlantic cod reflects past demographic processes driven by major historical events (such as oscillations in sea level) and subsequent gene flow rather than contemporary fluctuations in stock abundance. Our results indicate that historical and contemporaneous anthropogenic pressures such as commercial fisheries have had little impact on mitogenomic diversity in a wide-spread marine species with high gene flow such as Atlantic cod. These observations do not contradict evidence that overfishing has had negative consequences for the abundance of Atlantic cod and the importance of genetic variation in implementing conservation strategies. Instead, these observations imply that any measures toward the demographic recovery of Atlantic cod in the eastern Atlantic, will not be constrained by recent loss of historical mitogenomic variation.
Extreme philopatry and genetic diversification at unprecedented scales in a seabird
Scientific Reports, 2021
Effective conservation requires maintenance of the processes underlying species divergence, as well as understanding species’ responses to episodic disturbances and long-term change. We explored genetic population structure at a previously unrecognized spatial scale in seabirds, focusing on fine-scale isolation between colonies, and identified two distinct genetic clusters of Barau’s Petrels (Pterodroma baraui) on Réunion Island (Indian Ocean) corresponding to the sampled breeding colonies separated by 5 km. This unexpected result was supported by long-term banding and was clearly linked to the species’ extreme philopatric tendencies, emphasizing the importance of philopatry as an intrinsic barrier to gene flow. This implies that loss of a single colony could result in the loss of genetic variation, impairing the species’ ability to adapt to threats in the long term. We anticipate that these findings will have a pivotal influence on seabird research and population management, focusi...
Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations. Across island systems, contemporary patterns of genetic diversity reflect complex population demography, including colonisation events, bottlenecks, gene flow and genetic drift. Here, we investigate whether island founder events have prolonged effects on genome-wide diversity and runs of homozygosity (ROH) distributions, using whole genome resequencing from six populations across three archipelagos of Berthelot’s pipit (Anthus berthelotii) - a passerine which has undergone island speciation relatively recently. Pairwise sequential Markovian coalescent (PSMC) analyses estimated divergence from its sister species approximately two million years ago. Results indicate that all Berthelot’s pipit populations had shared ancestry until approximately 50,000 years ago, when the Madeiran archipelago populations were founded, while the Selvagens were colonised within the last 8,000 years. We...
Biological Reviews, 2020
Elucidating the factors underlying the origin and maintenance of genetic variation among populations is crucial for our understanding of their ecology and evolution, and also to help identify conservation priorities. While intrinsic movement has been hypothesized as the major determinant of population genetic structuring in abundant vagile species, growing evidence indicates that vagility does not always predict genetic differentiation. However, identifying the determinants of genetic structuring can be challenging, and these are largely unknown for most vagile species. Although, in principle, levels of gene flow can be inferred from neutral allele frequency divergence among populations, underlying assumptions may be unrealistic. Moreover, molecular studies have suggested that contemporary gene flow has often not overridden historical influences on population genetic structure, which indicates potential inadequacies of any interpretations that fail to consider the influence of history in shaping that structure. This exhaustive review of the theoretical and empirical literature investigates the determinants of population genetic differentiation using seabirds as a model system for vagile taxa. Seabirds provide a tractable group within which to identify the determinants of genetic differentiation, given their widespread distribution in marine habitats and an abundance of ecological and genetic studies conducted on this group. Herein we evaluate mitochondrial DNA (mtDNA) variation in 73 seabird species. Lack of mutation-drift equilibrium observed in 19% of species coincided with lower estimates of genetic differentiation, suggesting that dynamic demographic histories can often lead to erroneous interpretations of contemporary gene flow, even in vagile species. Presence of land across the species sampling range, or sampling of breeding colonies representing ice-free Pleistocene refuge zones, appear to be associated with genetic differentiation in Tropical and Southern Temperate species, respectively, indicating that long-term barriers and persistence of populations are important for their genetic structuring. Conversely, biotic factors commonly considered to influence population genetic structure, such as spatial segregation during foraging, were inconsistently associated with population genetic differentiation. In light of these results, we recommend that genetic studies should consider potential historical events when identifying determinants of genetic differentiation among populations to avoid overestimating the role of contemporary factors, even for highly vagile taxa.
Late Holocene range collapse in a former British seabird species
Aim To determine the taxonomic identity of zooarchaeological gadfly petrel (Pterodroma) specimens from northern Europe, in order to investigate whether an unknown, now-extinct Pterodroma species formerly occurred in this region, or whether extant north-east Atlantic gadfly petrel populations now restricted to the Macaronesian Islands formerly had a much wider Holocene distribution. Location Zooarchaeological Pterodroma material from the Hebrides, Scotland, was compared with modern-day material from the Madeira and Cape Verde archipelagos (Macaronesia) and a global Pterodroma sample. Methods We employed techniques for ancient DNA analysis to amplify mito- chondrial cytochrome b sequence data from an Iron Age Scottish Pterodroma specimen. Bayesian phylogenetic analyses were applied to assess the phylogenetic relationship between these ancient sequence data and extant Pterodroma taxa. Results The Scottish Pterodroma sample is phylogenetically distinct from living Macaronesian populations and from all other extant Pterodroma taxa. Although it is phylogenetically placed outside any single Macaronesian taxon, it is most closely related to the P. feae–deserta complex, and the level of sequence diver- gence between the Scottish Pterodroma and Macaronesian populations is lower than that observed between any two extant global Pterodroma taxa. The extinct north Atlantic gadfly petrels are therefore not distinct at the species level from these surviving populations, and instead form part of the young evolutionary radiation represented today by recently divergent Pterodroma populations on Bu- gio and Cape Verde, which can all be interpreted as conspecific. Main conclusions Our results suggest that surviving Macaronesian P. feae– deserta populations represent the final remnant of a wider Holocene distribu- tion of this species complex, with the Madeira and Cape Verde archipelagos constituting the final sanctuary of Pterodroma in the north Atlantic following late Holocene extirpation of more northerly colonies possibly associated with human-mediated invasive mammal introduction across northern Europe. Mac- aronesia may therefore constitute a ‘museum’ of diversity rather than a ‘cradle’ of evolution for Atlantic Pterodroma. Keywords Ancient DNA, birds, extinct, gadfly petrel, Macaronesia, phylogeography, Pterodroma, range collapse, Scotland, zooarchaeology.