Endangered subspecies of the reed bunting (Emberiza schoeniclus witherbyi and E. s. lusitanica) in Iberian Peninsula have different genetic structures

In the Iberian Peninsula, populations of two subspecies of the Reed Bunting Emberiza schoeniclus have become increasingly fragmented during the last decades when suitable habitats have been lost and/or the populations have gone extinct. Presently, both subspecies are endangered. We estimated the amount of genetic variation and population structure in order to define conservation units and management practices for these populations. We found that the subspecies lusitanica has clearly reduced genetic variation in nuclear and mitochondrial markers, has a drastically small effective population size and no genetic differentiation between populations. In contrast, the subspecies witherbyi is significantly structured, but the populations still hold large amounts of variation even though the effective population sizes are smaller than in the non-endangered subspecies schoeniclus. We suggest several management units for the Iberian populations. One unit includes subspecies lusitanica as a whole; the other three units are based on genetically differentiated populations of witherbyi. The most important genetic conservation measure in the case of lusitanica is to preserve the remaining habitats in order to at least maintain the present levels of gene flow. In the case of the three management units within witherbyi, the most urgent conservation measure is to improve the habitat quality to increase the population sizes.This project would not have been possible without the help of many people, among them A. Rodriguez, D. Bigas, P. Vicens, J. Segura, M. Suarez, J. L. Martinez, V. Urios, M. Rebassa, C. Torralvo, J. L. Hernandez, M. Carregal, P. Alcazar, J. L. Canto, J. Ramirez,, D. Alonso, J. Arizaga, F. Arcos, H. Rguibi, Acciona-Trasnmediterranea, and many others who helped us with the difficult task of sampling Reed Buntings and who sent us their samples. We apologize if we have forgotten someone. "Arcea Xestion de Recursos Naturais S. L." was of inestimable value in obtaining most of the samples from Galicia in 2008, in getting funding from the "Xunta de Galicia", and in helping us with the discussion of the results. We would like to thank the authorities of Daimiel National Park, Marjal Pego-Oliva Natural Park, S'Albufera de Mallorca Natural Park, Delta de L'Ebre Natural Park, "Consejeria de Medio Ambiente y Desarrollo Rural de Castilla La Mancha", "Servicio de Conservacion de la Diversidad del Gobierno de Navarra", "Direccion Xeral de Conservacion da Natureza de la Xunta Galicia and "Servei de Conservacio de la Biodiversitat de la Generalitat Valenciana" for the facilities to work in protected areas and for the appropriate permits to obtain the samples. The people from these protected areas were always very nice and helped us with the fieldwork. This study was funded by projects CGL2005-02041/BOS of the "Ministerio de Educacion y Ciencia" of Spain, and SC000207, Orden 14-12-2005 of the "Consejeria de Medio Ambiente y Desarrollo Rural de la Junta de Castilla La Mancha", Spain, through the "Ayudas para la realizacion de actuaciones de apoyo a la conservacion de las areas y recursos naturales protegidos, Orden 14-12-2005". The "Direccion Xeral de Conservacion da Natureza de la Xunta de Galicia", Spain, funded part of the fieldwork in NW Iberian Peninsula during the development of the Recovery plan for Emberiza schoeniclus lusitanica in Galicia. The experiments comply the current laws of the countries (Spain, Portugal and Finland) where they were done.Kvist, L.; Ponnikas, S.; Belda Perez, EJ.; Encabo, I.; Martinez, E.; Onrubia, A.; Hernandez, JM.... (2011). Endangered subspecies of the reed bunting (Emberiza schoeniclus witherbyi and E. s. lusitanica) in Iberian Peninsula have different genetic structures. 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Establishing conservation management for avian threatened species

Abstract The protection of endangered species requires knowledge about the habitat requirements and the genetic issues related to the population viability. In this doctoral thesis, I defined the breeding habitat features of the Finnish populations of the Golden Eagle (Aquila chrysaetos) and the Peregrine Falcon (Falco peregrinus) by applying habitat suitability modelling. Secondly, I studied the conservation genetic issues of the Finnish population of the White-tailed Eagle (Haliaeetus albicilla) and the two Reed Bunting subspecies Emberiza schoeniclus witherbyi and E.s. lusitanica met in the Iberian Peninsula. All study populations are classified as threatened according to IUCN classification and they have experienced declines in population sizes in recent history. My results from habitat suitability models showed that human-induced changes in habitat threaten the Golden Eagle in Finland. The relative suitability for the species presence dropped to zero when the proportion of human altered landscape (agricultural or urbanized areas) in the core of the breeding habitat (4 km2) was more than 5%. Models further showed that habitat structure influences breeding habitat selection of the Peregrine Falcon, as it favours well-connected areas of open peatlands. Therefore, fragmentation (i.e., decreasing the connectivity) of open peatlands decreases the habitat quality for the species. The White-tailed Eagle has recovered mainly through local growth, but my results suggest that gene flow from neighbouring populations has had an impact as well, and has enhanced the genetic viability of the Finnish population. The current structure of the two subpopulations (one along the Baltic Sea coast line and another inland in Northern Finland) results mainly from the species’ ecology (i.e., philopatric behaviour), not from the recent population bottlenecks. The effective population size estimate of the coastal subpopulation of White-tailed Eagle was below the critical size needed to maintain evolutionary potential. The estimates of the effective population sizes for E.s. lusitanica and E.s. witherbyi and inland subpopulation of White-tailed Eagle were close or below the critical level of 50, which makes them prone to losing fitness due to inbreeding depression in the short term. Therefore, these study populations need to increase in size in order to secure population viability in the future.Tiivistelmä Ihmisen aiheuttamat elinympäristöjen muutokset uhkaavat biodiversiteettiä kasvattamalla yhä useampien eliölajien sukupuuttoriskiä. Tehokkaat suojelutoimenpiteet edellyttävät tietoa uhanalaisten lajien elinympäristövaatimuksista sekä populaation elinkyvylle keskeisistä geneettisistä tekijöistä. Tarkastelen väitöskirjatyössäni maakotkan (Aquila chrysaetos) sekä muuttohaukan (Falco peregrinus) Suomen populaatioiden pesimäympäristön piirteitä maisemaekologisen mallinnuksen avulla. Toiseksi tarkastelen Suomen merikotkapopulaation (Haliaeetus albicilla) sekä Iberian niemimaalla esiintyvien pajusirkun alalajien Emberiza schoeniclus witherbyin ja E.s. lusitanican suojelun kannalta tärkeitä geneettisiä tekijöitä. Kaikki tutkimuspopulaatiot ovat uhanalaisia ja ne ovat kärsineet voimakkaista kannan pienenemisistä. Maisemaekologiset mallit osoittivat maakotkan välttävän ihmisen muokkaamaa ympäristöä (maatalousalueet ja rakennetut alueet). Lajin esiintymistodennäköisyys laski nopeasti nollaan, kun ihmisen muokkaaman ympäristön osuus nousi yli 5 prosenttiin pesimäympäristön ydinalueella (4 km2). Mallit osoittivat maiseman rakenteen vaikuttavan muuttohaukan habitaatinvalintaan, sillä se suosi pesimäympäristönään kytkeytyneitä avosoita. Avosoiden pirstoutuminen (l. kytkeytyneisyyden väheneminen) vähentää näin ollen muuttohaukan pesimäympäristön laatua. Merikotkapopulaatio on toipunut pääosin paikallisen kasvun myötä, mutta tulokseni viittaavat myös siihen, että geenivirta naapurimaiden populaatioista on lisännyt Suomen populaation geneettistä muuntelua. Nykyinen rakenne (rannikon ja Lapin alapopulaatiot) on seurausta lajin synnyinpaikkauskollisuudesta, ei niinkään populaatiokoon romahduksista. Rannikon merikotkapopulaation efektiivinen koko jäi alle kriittisen rajan, joka tarvitaan evolutiivisen potentiaalin säilymiselle. Pajusirkun alalajien sekä Lapin merikotkapopulaation efektiiviset populaatiokoot olivat lähellä kriittisenä pidettyä 50:tä tai jäivät alle, joten ne ovat vaarassa menettää kelpoisuutta sukusiitosdepression seurauksena lyhyellä aikavälillä. Sekä pajusirkun alalajien että merikotkapopulaatioiden tulee sen vuoksi kasvaa säilyäkseen elinvoimaisina tulevaisuudessa

Turnover and post‐bottleneck genetic structure in a recovering population of Peregrine Falcons Falco peregrinus

Abstract Dispersal is a process that increases genetic diversity and genetic connectivity of populations. We studied the turnover rate of breeding adults and genetic population structure to estimate dispersal in Peregrine Falcons in Finland. We used relatedness estimates among Finnish Peregrine Falcons over a 5‐year period, genotyping over 500 nestlings with 10 microsatellite loci to reveal the rate of turnover. Our results reveal a high turnover rate (21.7%) that does not seem to be correlated with the breeding success of the previous year. The extent of population genetic structure and diversity, and possible signs of the population crash during the 1970s, was assessed with a reduced dataset, excluding relatives. We found genetic diversity to be similar to previously studied falcon populations (expected heterozygosity of 0.581) and no population genetic structuring among our sampled populations. We did not find a genetic imprint of the past population bottleneck that the Finnish Peregrine population experienced. We conclude that high dispersal rates are likely to have contributed to maintaining genetic diversity across the landscape, by mixing individuals within the species’ distribution in Finland and thus preventing genetic structuring and negative effects associated with the population decline in the 1970s

Extreme variation in recombination rate and genetic diversity along the Sylvioidea neo-sex chromosome

Abstract Recombination strongly impacts sequence evolution by affecting the extent of linkage and the efficiency of selection. Here, we study recombination over the Z chromosome in great reed warblers (Acrocephalus arundinaceus) using pedigree-based linkage mapping. This species has extended Z and W chromosomes (“neo-sex chromosomes”) formed by a fusion between a part of chromosome 4A and the ancestral sex chromosomes, which provides a unique opportunity to assess recombination and sequence evolution in sex-linked regions of different ages. We assembled an 87.54 Mbp and 90.19 cM large Z with a small pseudoautosomal region (0.89 Mbp) at one end and the fused Chr4A-part at the other end of the chromosome. A prominent feature in our data was an extreme variation in male recombination rate along Z with high values at both chromosome ends, but an apparent lack of recombination over a substantial central section, covering 78% of the chromosome. The nonrecombining region showed a drastic loss of genetic diversity and accumulation of repeats compared to the recombining parts. Thus, our data emphasize a key role of recombination in affecting local levels of polymorphism. Nonetheless, the evolutionary rate of genes (dN/dS) did not differ between high and low recombining regions, suggesting that the efficiency of selection on protein-coding sequences can be maintained also at very low levels of recombination. Finally, the Chr4A-derived part showed a similar recombination rate as the part of the ancestral Z that did recombine, but its sequence characteristics reflected both its previous autosomal, and current Z-linked, recombination patterns

Consequences of partially recessive deleterious genetic variation for the evolution of inversions suppressing recombination between sex chromosomes

Abstract The evolution of suppressed recombination between sex chromosomes is widely hypothesized to be driven by sexually antagonistic selection (SA), where tighter linkage between the sex-determining gene(s) and nearby SA loci is favored when it couples male-beneficial alleles to the proto-Y chromosome, and female-beneficial alleles to the proto-X. Despite limited empirical evidence, the SA selection hypothesis overshadows several alternatives, including an incomplete but often-repeated “sheltering hypothesis” that suggests that expansion of the sex-linked region (SLR) reduces homozygous expression of partially recessive deleterious mutations at selected loci. Here, we use population genetic models to evaluate the consequences of deleterious mutational variation for the evolution of neutral chromosomal inversions expanding the SLR on proto-Y chromosomes. We find that SLR-expanding inversions face a race against time: lightly loaded inversions are initially beneficial, but eventually become deleterious as they accumulate new mutations, and must fix before this window of opportunity closes. The outcome of this race is strongly influenced by inversion size, the mutation rate, and the dominance coefficient of deleterious mutations. Yet, small inversions have elevated fixation probabilities relative to neutral expectations for biologically plausible parameter values. Our results demonstrate that deleterious genetic variation can plausibly drive recombination suppression in small steps and would be most consistent with empirical patterns of small evolutionary strata or gradual recombination arrest

Turnover and natal dispersal in the Finnish golden eagle (Aquila chrysaetos) population

Abstract Estimating turnover in a population provides information on population dynamics, such as dispersal and mortality. Dispersal increases genetic diversity and affects the genetic structure. Golden eagles are monogamous, tend to mate for life, and have strong nest site fidelity, which suggests low turnover rates. Here, we first studied genetic diversity and population structure in the Finnish golden eagle population using 11 microsatellite loci and a fragment of a mitochondrial DNA control region. We found no notable changes in genetic diversity during the 15-year study period and did not discover any population structure. Then, we examined the turnover rate using chick genotypes (N = 935) by estimating relatedness between chicks born in the same territory in different years. The results showed a turnover rate of 23%, which correlated with the breeding success of the previous year. Similarly, in the absence of turnover, the pair changed nest sites within a territory after an unsuccessful breeding. In addition, our dataset also revealed natal dispersal of ten individuals. Natal dispersal distance was 110 km on average (median 98 km); however, the distance seemed to vary depending on geographical location, being greater in Northern Finland than in Southern Finland

Dense sampling of bird diversity increases power of comparative genomics

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity(1-4). Sparse taxon sampling has previously been proposed to confound phylogenetic inference(5), and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families-including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species. A dataset of the genomes of 363 species from the Bird 10,000 Genomes Project shows increased power to detect shared and lineage-specific variation, demonstrating the importance of phylogenetically diverse taxon sampling in whole-genome sequencing.Peer reviewe

Author Correction: Dense sampling of bird diversity increases power of comparative genomics

In Supplementary Table 1 of this Article, 23 samples (B10K-DU-029-32, B10K-DU-029-33, B10K-DU-029-36 to B10K-DU-029-44, B10K-DU- 029-46, B10K-DU-029-47, B10K-DU-029-49 to B10K-DU-029-53, B10K-DU- 029-75 to B10K-DU-029-77, B10K-DU-029-80, and B10K-DU-030-03; styled in boldface in the revised table) were assigned to the incorrect institution. Supplementary Table 1 has been amended to reflect the correct source institution for these samples, and associated data (tissue, museum ID/source specimen ID, site, state/province, latitude, longitude, date collected and sex) have been updated accordingly. The original table is provided as Supplementary Information to this Amendment, and the original Article has been corrected online