Genetic consequences of intensive management in game birds

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Abstract

Introduction of wildlife for game restocking is one major pathway of genetic homogenization. The red-legged partridge (Alectoris rufa, Phasianidae), a small game bird native to south-western Europe, is in high demand by hunters and natural populations are constantly supplemented by commercial stocks of captive-bred individuals. Also, in recent years human-mediated hybridization with congeneric chukar partridges (Alectoris chukar: Greece, Cyprus, from Middle East to East Asia) has been frequently documented in the wild and in captivity. This study attempts to evaluate the genetic consequences of intensive captive breeding and restocking in the A. rufa species. We investigated A. rufa genetic diversity by making comparisons in both a spatial (across the entire species’ range) and a temporal framework. We accomplished this latter by comparing modern vs. ancient partridges resident in museums and collected 1856–1934, well before supplemental stocking became common. Using mtDNA we found significant changes in the haplotype profile of modern vs. ancient A. rufa, and widespread introgression with chukar genes across the entire species range only in modern representatives, with the relevant exception of Corsican populations. However, Random Amplified Polymorphic DNA (RAPD), as opposed to microsatellite DNA markers, showed also modern Corsican populations to harbour many A. rufa × A. chukar hybrids. We conclude that captive breeding programs should make strict use of time-saving and comparatively low cost DNA barcodes to minimize genetic pollution, such as those provided by diagnostic RAPD markers. We also recommend that the active ban on import of exotics and/or hybrids be extended to non-local populations. Altogether this would represent a substantial step forward to preserve A. rufa as well as other game species subjected to similar intensive management.

Introduction

Biotic homogenization – an increase in the spatial similarity of a biological variable over time (Olden et al., 2004) – is a process often driven by a breakdown of dispersal barriers through anthropogenic means, which leads to the gradual replacement of native biotas by locally expanding invasives (McKinney and Lockwood, 1999, Olden and Poff, 2003). Although homogenization is now considered one of the most prominent forms of biotic impoverishment worldwide (Sax and Gaines, 2003), it is not a new fact (Vermeij, 1991). Recently, humans have accelerated this process through global commerce (Mack et al., 2000). This has minimized distinctiveness among regions, which is essential to preserve biodiversity through allopatric speciation (Olden et al., 2004).

Genetic homogenization is a serious threat to integrity of endemic gene pools as it reduces the spatial component of variability among populations. Suitable quantification requires sufficient sample size allowing comparative analysis of diversity not only in a spatial but also in a temporal framework, using a variety of metrics such as, for example, allelic composition, genotype frequency and Wright’s (1951)F-statistics (Olden et al., 2004).

Relocation of wildlife for game management can promote genetic admixture among different taxa (Rhymer and Simberloff, 1996, Frankham et al., 2002, Delibes-Mateos et al., 2008, Spear and Chown, 2008). Releases of captive specimens often result in introgressive hybridization with exotics or with domesticated relatives, and loss of taxonomic distinctness as well as of important adaptive behavioural traits (e.g., Deregnacourt et al., 2002, Latch et al., 2006, Muñoz-Fuentes et al., 2007, Randi, 2008). When homogenization due to commercial trade is examined across taxa, Phasianidae (order Galliformes) appears as one of the most problematic groups (Romagosa et al., 2009). Although there are ample examples of natural populations of hunted species that are sustained through natural reproduction (e.g., sharp-tailed grouse, Tympanuchus phasianellus, Phasianidae), often socio-economic reasons associated with hunting require large numbers of birds to shoot that can be provided only by supplementing natural breeding with artificial rearing and massive relocation (e.g., in the red-legged partridge, Alectoris rufa). In these cases management often occurs without regard for genetic similarity or geographic origin of farmed stocks. Hence, both adverse genetic changes in captivity as well as hybridization jeopardize the ability of populations to survive when returned to the wild (Ford, 2002, Keane et al., 2005, Frankham, 2008). For instance, whereas A. rufa restocked population of Pianosa Island (Italy) survives at high density within the limits of a National Park and in the absence of predators (Barbanera et al., 2005), all Italian A. rufa reintroductions with farm-bred birds failed in the absence of continuous releases. Survival is affected by low fitness and poor habitat suitability of the reintroduction areas, especially small size and isolation. Such factors make gamekeeping necessary, including predator reduction and supplemental food in winter (e.g., Meriggi et al., 2007).

The red-legged partridge (A. rufa, Phasianidae) is a small-sized galliform hunted throughout its entire range (Iberian Peninsula, France and Italy: Madge and McGowan, 2002). Three subspecies are recognised: A. rufa hispanica (Seoane, 1894) in northern and central Portugal (Madeira included) and north-western Spain, A. rufa intercedens (A E Brehm, 1858) in southern and eastern Spain (Mallorca included), and A. rufa rufa (Linnaeus, 1758) in Italy and France (Elba and Corsica included) (Madge and McGowan, 2002). This species is in such high demand by hunters that commercial stocks of captive-bred individuals constantly supplement natural populations. For instance, in the Iberian Peninsula four million birds are shot and two million birds are released every year (Delibes, 1992). In recent years, human-mediated hybridization with congeneric chukar partridges (Alectoris chukar: Greek islands, Cyprus, and from Middle East to East Asia) has been frequently documented (Iberian Peninsula: e.g., Dias, 1992, Gonzalez et al., 2005, Fresno et al., 2008, Tejedor et al., 2008; France and Italy, e.g., Baratti et al., 2004, Barbanera et al., 2005, Barilani et al., 2007). In captivity the chukar is the most prolific Alectoris breeder, and crossing with red-legged partridges is productive.

This study attempts to evaluate the genetic consequences of intensive captive breeding and restocking in the A. rufa species. In order to pursue a more global perspective than that of previous studies [as suggested by Olden et al. (2004)] we investigated A. rufa genetic diversity by making comparisons in both a spatial (across the species’ range) and a temporal framework. We accomplished this latter by comparing modern vs. ancient red-legged partridges resident in museums and collected 1856–1934, well before farmed stocks for supplemental stocking became common (after World War II: Goodwin, 1986, Blanco-Aguiar et al., 2008). Given the degraded nature of ancient DNA, we utilized mitochondrial (mtDNA) rather than nuclear DNA (nDNA) because of its much higher DNA template copy number. We disclosed intra-specific genetic admixture and loss of ancient A. rufa mtDNA genotypes, as well as recent introgression with chukar genes throughout the species’ range, with the relevant exception of wild Corsican populations. We gain insight into the Corsican A. rufa using microsatellite and Random Amplified Polymorphic DNA (RAPD) markers (cf., Negro et al., 2001, Baratti et al., 2004, Barbanera et al., 2005, Barbanera et al., 2007, Barbanera et al., 2009a, Barbanera et al., 2009b, Barilani et al., 2006, Barilani et al., 2007). We found A. rufa × A. chukar hybrids in all modern populations, thus providing evidence for genetic pollution across the entire A. rufa range.

Section snippets

Biological sampling

We acquired slivers of toe pads (n = 54) of ancient red-legged partridges resident in European and US museums (Supplementary Table S1), and collected 1856–1934 from the Iberian Peninsula (n = 18, Madeira and Mallorca included), France (n = 12, Corsica included) and Italy (n = 24, Elba included). Between 2003 and 2008 we collected samples of modern A. rufa representatives (n = 194) from Iberian Peninsula (n = 56, Mallorca included), France (n = 82: of these, 48 from Corsica) and Italy (n = 56, Elba included) (

Mitochondrial DNA genotyping

We successfully amplified the Cyt-b gene of all (n = 194) modern and of 47 ancient red-legged partridges (sample size, n = 54) (Supplementary Table S1). The mtDNA sequences conformed to the neutral model of evolution (Tajima’s D = 0.205; P = 0.65). The alignment revealed that all ancient specimens hold 100% A. rufa mitochondrial lineage (0% A. chukar), whereas, among modern representatives, 48.2% (n = 27) of Italian, 29.4% of French (mainland; n = 10) and 7.2% of Iberian (n = 4) hold that of A. chukar (two

Discussion

Recent molecular genetic studies have disclosed many isolated cases of human-mediated A. chukar introgression into modern A. rufa genome (Baratti et al., 2004, Barbanera et al., 2005, Barilani et al., 2007, Fresno et al., 2008, Tejedor et al., 2008). However, only Blanco-Aguiar et al. (2008) compared modern vs. museum A. rufa by means of restriction enzyme analysis of mtDNA Cyt-b of Iberian representatives. These specimens were collected 1960–1980, much later than our ancient samples. They

Acknowledgements

For ancient A. rufa samples we thank: A. Cibois, Natural History Museum of Geneva, Geneva, Switzerland; S. Gellini, Ferrante Foschi Ornithological Museum, Forlì, Italy; K. van Grouw, The Natural History Museum, Tring, UK; I. Heynen, State Museum of Natural History, Stuttgart, Germany; C. Marangoni, Municipal Museum of Zoology, Rome, Italy; A. Mennucci, Ornithological Museum of San Gimignano, Siena, Italy; P. Sweet, American Museum of Natural History, New York, USA; D. Willard, Field Museum of

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      For the conservation of natural populations of red-legged partridge, the release into the wild of hybrid specimens can be extremely dangerous [7]. Although hybrids are less adapted to the field, uncontrolled restocking may lead to a widespread introgression of foreign genetic material into locally adapted red-legged partridge populations [1,5,6], eventually causing the extinction of the red-legged partridge as a wild species [8]. For this reason, the administrations with competences in game management and conservation of nature should establish a control system for both farms and natural environments to preserve the genetics of red-legged partridge wild populations.

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