The genetic structure of the European breeding populations of a declining farmland bird, the ortolan bunting (Emberiza hortulana), reveals conservation priorities

Abstract

Anthropogenic activities, such as agricultural intensification, caused large declines in biodiversity, including farmland birds. In addition to demographic consequences, anthropogenic activities can result in loss of genetic diversity, reduction of gene flow and altered genetic structure. We investigated the distribution of the genetic variation of a declining farmland and longdistance migratory bird, the ortolan bunting Emberiza hortulana, across its European breeding range to assess the impact of human-driven population declines on genetic diversity and structure in order to advise conservation priorities. The large population declines observed have not resulted in dramatic loss of genetic diversity, which is moderate to high and constant across all sampled breeding sites. Extensive gene flow occurs across the breeding range, even across a migratory divide, which contributes little to genetic structuring. However, gene flow is asymmetric, with the large eastern populations acting as source populations for the smaller western ones. Furthermore, breeding populations that underwent the largest declines, in Fennoscandia and Baltic countries, appear to be recently isolated, with no gene exchange occurring with the eastern or the western populations. These are signs for concern as declines in the eastern populations could affect the strength of gene flow and in turn affect the western populations. The genetic, and demographic, isolation of the northern populations make them particularly sensitive to loss of genetic diversity and to extinction as no immigration is occurring to counter-act the drastic declines. In such a situation, conservation efforts are needed across the whole breeding range: in particular, protecting the eastern populations due to their key role in maintaining gene flow across the range, and focussing on the northern populations due to their recent isolation and endangered status.

Unravelling migration connectivity reveals unsustainable hunting of the declining ortolan bunting

“…We used δ 2 H f of ortolan buntings to identify the probable wintering grounds of breeding populations sampled across Europe ( n = 535 individuals) and the probable breeding grounds of migrants captured along fall migration flyways ( n = 152 individuals). Last, we genotyped 266 migrant buntings captured in France along the Atlantic flyway to assign these migrants to potential breeding populations, owing to the mapped genetic structure of breeding populations across the continent performed with 24 variable microsatellite loci ( n = 575 individuals from 26 breeding sites from Spain throughout Europe to eastern European Russia) ( 14 ).…”

“…S4). This northern cluster is genetically isolated with almost no emigration or immigration from Western or Eastern Europe ( 14 ), and the breeding populations there have declined by almost 5% annually (53% from 2000 to 2014; data file S1).…”

“…The aim of the genetic part of the research program was to determine the genetic structure of European breeding populations [see ( 14 ) for additional details] and to assign autumn migrants captured on the western flyway (southwest France) and the eastern flyway (Kuwait and Israel) to genetic breeding groups/areas.…”

“…S4). Further details on the genetic study can be found in ( 14 ), including pairwise FST (fixation index) between populations and estimates of contemporary gene flow.…”

Towards inclusion of genetic diversity measures into IUCN assessments: a case study on birds

“…Variability estimated using molecular markers not only helps to distinguish genetically distinct populations that may be vulnerable to environmental changes (e.g., Lee and Mitchell-Olds, 2011;Hansen et al, 2012;Limborg et al, 2012;Munday et al, 2013;Razgour et al, 2018) but also infers phylogenetic relationships between individuals both within and between species, reconstructing genealogies and gathering information on inbreeding rates (e.g., Zollinger et al, 2012;McCormack et al, 2013;Lyu et al, 2018). The current use of microsatellite markers in biodiversity conservation studies is particularly useful to address issues related to the conservation genetics of various bird species (e.g., Moura et al, 2017;Houston et al, 2018;Moussy et al, 2018;Stojanovic et al, 2018). Conservation Genetics has been defined as the discipline that applies genetic concepts and tools, including molecular markers, to small populations to reduce their risk of extinction (Frankham et al, 2002;Allendorf et al, 2012).…”