Genome-wide markers redeem the lost identity of a heavily managed gamebird

Abstract

Heavily managed wildlife may suffer from genetic homogenization and reshuffling of locally adapted genotypes with non-native ones. This phenomenon often affects natural populations by reducing their evolutionary potential and speeding up the ongoing biodiversity crisis. For decades, the red-legged partridge (Alectoris rufa), an intensively managed gamebird of conservation concern and considerable socio-economic importance, has been subjected to extensive releases of farm-reared hybrids with the chukar partridge (Alectoris chukar) and translocations irrespective of subspecific affinity. These practices have led to serious concerns that the genetic integrity and biogeographic structure of most red-legged partridge populations are irreversibly affected, as suggested by previous studies based on few genetic markers. Using over 168 000 genome-wide loci and a sampling across the entire A. rufa range, we detected unexpectedly limited and spatially uneven chukar introgression as well as significant intraspecific structure. We demonstrate that species widely feared to have irretrievably lost their genetic identity are likely to be much less affected by unsuitable management practices than previously assumed. Our results spell the need for a radical re-think on animal conservation, possibly restoring native status to populations long treated as compromised. Our study exemplifies how the application of innovative conservation-genomic methods is key to solving wildlife management problems dealing with introgressive hybridization worldwide.

Keywords: Alectoris rufa; evolutionary potential; galliformes; genetic homogenization; introgression; wildlife management.

Figure 1.

Distribution map of A. rufa and A. chukar (inset) with sampling localities and Admixture results at K = 3 based on 168 675 SNPs. The ranges of each taxon are given in different colours: A. chukar, white; A. r. rufa, red; A. r. intercedens, light blue; A. r. hispanica, dark blue [18]. Dotted lines indicate A. chukar distribution across the Eastern Mediterranean islands. Equal-sized pie charts show genotype assignment across different sampling localities (electronic supplementary material, dataset S1) with colours indicating allelic contributions typical of different genetic groups: white for A. chukar; yellow and green for A. rufa. Pictures of the two species are shown in the top left corner of their respective maps (author: F.B.). PT, Portugal; SP, Spain; FR, France; UK, United Kingdom; IT, Italy. (Online version in colour.)

Figure 2.

Distribution map of A. rufa with sampling localities and Admixture results at K = 3 based on 138 874 SNPs. The ranges of morphological subspecies are given in different colours: A. r. rufa, red; A. r. intercedens, light blue; A. r. hispanica, dark blue [18]. Equal-sized pie charts show genotype assignment across different sampling localities (electronic supplementary material, dataset S1) with colours indicating allelic contributions typical of different genetic groups: red for nominate A. r. rufa; blue for Iberian A. r. intercedens and A. r. hispanica; lilac for populations with a homogenized allelic contribution of captive-released stocks. PT, Portugal; SP, Spain; FR, France; UK, United Kingdom; IT, Italy. (Online version in colour.)

Figure 3.

(a) Principal component analysis based on 168 675 SNPs extracted from restriction-associated DNA comparing A. rufa (circles, n = 75) and A. chukar (squares, n = 6). The colour scheme used is consistent with taxon distributions as shown in figure 1: A. chukar, white; A. r. rufa, red; A. r. intercedens, light blue; A. r. hispanica, dark blue. Individuals from Corsica and Elba Island (highly preserved A. r. rufa populations) as well as Pianosa Island (hosting an A. rufa population heavily admixed with A. chukar) are delimited by ovals. The arrow indicates captive individuals from Scarlino and Chambretaud (bordered black; electronic supplementary material, dataset S1). (b) Principal component analysis based on 138 874 SNPs extracted from restriction-associated DNA showing the intraspecific structure of A. rufa (n = 75). The colour scheme used is consistent with taxon distribution shown in figure 1: A. r. rufa, red; A. r. intercedens, light blue; A. r. hispanica, dark blue. Individuals from Corsica and Elba Island as well as Pianosa Island are delimited by ovals. The names of morphological subspecies are placed beside the groups of individuals on the basis of their geographical origin. The arrows indicate geographical outliers (see Discussion) flagged with asterisks in the electronic supplementary material, figure S3 (bordered black; electronic supplementary material, dataset S1). (Online version in colour.)

Figure 4.

Manhattan plots showing genome-wide pairwise F_ST values between populations of interest. Dotted lines mark the threshold of F_ST = 0.6, above which differentiation is considered high. (a) Corsica versus others; (b) Elba Island versus others; (c) Pianosa Island versus others; (d) others versus others. NW Spain, northwestern Spain (Zamora, León, Cangas del Narcea: electronic supplementary material, dataset S1). The distinctive features of A. chukar introgression in Elba and Pianosa individuals are marked by yellow arrows. (Online version in colour.)