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Biological and Genetic Aspects Wild Boar UNIVERSITÀ DEGLI STUDI DI SASSARI Dissertation for the Degree of Doctor of Philosophy in Environmental Biology presented at Sassari University in 2015 XXVIII cycle Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations PH.D. CANDIDATE: Dr. Antonio Canu DIRECTOR OF THE SCHOOL: Prof. Marco Curini-Galletti SUPERVISOR: Dr. Massimo Scandura La presente tesi è stata prodotta nell’a*bito della scuola di dottorato in Scienze della "atura e delle sue Risorse dell’Università degli Studi di Sassari, a.a. $%'$/$%'(011-,,, ciclo+ con il supporto di una borsa di studio finanziata con le risorse del P.O.R. SARD !"A #.S. $%%&) $%'( ) Obiettivo co*petitività regionale e occupazione+ Asse ,- .apitale u*ano+ Linea di Attività l.(.'. Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations INDEX Abstract ........................................................................................................... 5 Riassunto ........................................................................................................... 7 Introduction ........................................................................................................... 9 First part - Hybridization between wild boar and domestic pig 33 Chapter I Are captive wild boar more introgressed than free-ranging wild 35 boar? Two case studies in Italy Chapter II Lack of polymorphism at MC1R wild-type allele and evidence of 47 domestic alleles introgression across European wild boar populations Chapter III Novel Y-chromosome STRs in Sus scrofa and their variation in 59 European wild boar and domestic pig populations Chapter IV Isolation by distance, by barrier and by resistance have shaped a 83 sharp genetic structure in a island wild boar population Chapter V Reproductive phenology and conception synchrony in a natural 121 wild boar population Second part - Hybridization between wol and dog 131 Chapter VI Do wolves and free-ranging wolf x dog hybrids share the same 133 food niche? First insights from Apennine mountains, Italy Chapter VII Video-scats: joining camera trapping and non-invasive genotyping 167 as a tool to confirm hybrid assessment and individual identification !onclusions ........................................................................................................... 185 Appendi" ........................................................................................................... 195 Ac#nowledgements ........................................................................................................... 209 Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations A$S%RA!% Nowadays, hybridization is recognized as a powerful evolutionary force promoting speciation and shaping adaptation, but also as a serious threat to the conservation of biodiversity. This thesis is focused on two cases of hybridization between wild and domestic conspecifics, whose effects are mostly unexplored. In Sus scrofa, I sought to expand knowledge about hybridization between wild boar and domestic pig. I investigated the main sources of domestic genes introgression, and assessed hybridization at neutral markers and functional genes at both local and European scale. I also developed a set of new uniparental markers for studying male-specific gene flow, and studied the reproductive phenology of wild populations. In Canis lupus, I investigated patterns of hybridization between wolf and domestic dog in an Italian mountain area, focusing on the assessment of introgression and the food habits of hybrids. As regards wild boar, I detected introgression all over Europe, also highlighting the role of breeding stations in spreading domestic genes across wild populations. With respect to wolf, a new approach was used to provide complementary (genetic and phenotypic) data on specific individuals and to support hybrid identification. A trophic niche overlap between wolves and hybrids was also proved. These studies can have relevant management implications, offering new elements of knowledge on different aspects of the hybridization in two worrisome species of the Italian fauna. Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations RIASS&N%' Più conosciamo il fenomeno dell'ibridazione, e più ci rendiamo conto del suo aspetto bivalente: da un lato, potente forza evolutiva che favorisce la speciazione; dall'altro, seria minaccia per la conservazione della biodiversità. Questa tesi si occupa in particolare dell'ibridazione tra conspecifici domestici e selvatici, un fenomeno i cui effetti sono lungi dall'esser compresi appieno. Nella prima parte del lavoro, mi sono concentrato sull'ibridazione tra maiale domestico e cinghiale (Sus scrofa). Cercando di chiarire quali fossero le principali fonti di introgressione di geni domestici nelle popolazioni selvatiche, e adottando sia marcatori molecolari neutrali che geni funzionali per rilevare introgressione su scala locale ed Europea. Ho inoltre collaborato allo sviluppo di nuovi marcatori a trasmissione patrilineare, ed allo studio della fenologia riproduttiva in popolazioni selvatiche di cinghiale. Nella seconda parte della tesi mi sono occupato dell'ibridazione tra lupo (Canis lupus) e cane in un'area dell'Appennino toscano, studiando l'entità del fenomeno e le abitudini alimentari degli ibridi. Per quanto riguarda il cinghiale, l'introgressione è risultata estesa a tutt'Europa, e nella sua diffusione si è rivelato importante il ruolo giocato dagli allevamenti. Relativamente al lupo, il nostro nuovo approccio ha fornito informazioni complementari su genetica e fenotipo di specifici individui, fondamentali per una più accurata identificazione degli ibridi. Abbiamo inoltre evidenziato una forte sovrapposizione della nicchia trofica tra ibridi e lupi, dunque una loro probabile competizione per le risorse. I risultati ottenuti possono offrire notevoli implicazioni gestionali, ampliando le conoscenze su diversi aspetti dell'ibridazione tra forma domestica e selvatica in due specie 'problematiche' della fauna italiana. Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations INTRODUCTION This thesis deals with various aspects of the complex phenomenon of hybridization, increasingly recognized as a powerful evolutionary force promoting speciation and shaping adaptation, but also posing a serious risk to the conservation of biodiversity. A special case of hybridization is that occurring between wild species and domestic conspecifics, a subject that deserves a special attention for its evolutionary and management implications. This thesis is focused on two cases of wild x domestic hybridization. The former part is focused on the hybridization between wild boar (Sus scrofa) and domestic pig (Sus scrofa domestica), while the second one deals with the crossbreeding between wolf (Canis lupus) and dog (C. lupus familiaris). Both genetic/methodological and biological aspects are touched, such as the identification of hybrids, the development of new molecular markers and investigations on the source of introgression, reproductive phenology of the species involved and ecological traits of hybrids. Hybridization and its effects on fitness Hybridization was defined as ‘interbreeding of individuals from genetically distinct populations, regardless of their taxonomic status’ (Rhymer & Simberloff, 1996), while 'introgression' refers to the movement of genes between genetically differentiated forms mediated by backcrossing (Avise 1994). Accordingly, introgressive hybridization refers to an exchange of genes between evolutionary lineages as opposed to hybridization yielding exclusively inviable or infertile offspring (Seehausen 2004). These broad definitions account for the fact that both inter- and intraspecific hybridization are relevant from a conservation perspective, both providing an extremely tough set of issues for conservation biologists. Hybridization and introgression are strongly increasing worldwide due to intentional and incidental translocations of plants and animals, habitat modifications (Allendorf et al. 2001), human pressure (Rutledge et al. 2012) and climate change (Garroway et al. 2010). Biological and genetic aspects of wild x domestic hybridization in wild boar and wolf populations For example, the introduction of plants and animals outside their native range, the creation of extensive areas of new habitats and the establishment of migration corridors have the effect of breaking down mechanisms of isolation between species and populations, generating opportunities for formerly allopatric taxa to meet and hybridize (Rhymer and Simberloff 1996; Stronen & Paquet 2013). Furthermore, a population decrease caused by anthropogenic factors can promote hybridization among species/populations because of the increased difficulty in finding mates (Allendorf & Luikart 2007). Mallet (2005) reported that at least 25% of plant species and 10% of animal species (6% of European mammals) are involved in hybridization and introgression with other species. This increasing anthropogenic hybridization is causing extinction of many taxa (species, subspecies and locally
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