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Crossing Species Boundaries the Hybrid Histories of the True Geese

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Crossing Species Boundaries The Hybrid Histories of the True Geese Jente Ottenburghs Thesis committee Promotors Prof. Dr. H.H.T. Prins Professor of Resource Ecology Wageningen University Prof. Dr. R.C. Ydenberg Professor of Behavioral Ecology Simon Fraser University, Canada Co-promotor Dr. H.J.W.C. Megens Assistant professor, Animal Breeding and Genetics Wageningen University Other members Dr J.W. Arntzen, Naturalis Biodiversity Centre, Leiden Prof. Dr B. Nolet, Netherlands Institute of Ecology, Wageningen Dr R. Reifova, University of Prague, Czech Republic Prof. Dr B.J. Zwaan, Wageningen University This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation. Crossing Species Boundaries The Hybrid Histories of the True Geese Jente Ottenburghs Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University & Research by the authority of the Rector Magnificus Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Thursday 8 December 2016 at 11 a.m. in the Aula. Jente Ottenburghs Crossing Species Boundaries: The Hybrid Histories of the True Geese, 266 pages. PhD thesis Wageningen University & Research, Wageningen, NL (2016) With references, with summaries in English and Dutch ISBN: 978-94-6257-978-1 DOI: 10.18174/393256 Abstract ABSTRACT Ottenburghs, J. (2016). Crossing Species Boundaries: The Hybrid Histories of the True Geese. PhD thesis, Wageningen University, the Netherlands. Hybridization, the interbreeding of different species, is a common phenomenon in birds: about 16% of bird species is known to have hybridized with at least one other species. Numerous avian hybrid zones have been studied from a morphological or genetic perspective, often documenting the interspecific exchange of genetic material by hybridization and backcrossing (i.e. introgression). The incidence of hybridization varies among bird orders with the Anseriformes (waterfowl: ducks, geese and swans) showing the highest propensity to hybridize. In this thesis, I provide a genomic per- spective on the role of hybridization in the evolutionary history of one particular an- seriform tribe, the Anserini or “True Geese”, which comprises 17 species divided over two genera: Anser and Branta . The diversification of this bird group took place in the late Pliocene and the early Pleistocene (between four and two million years ago), con- ceivably driven by a global cooling trend that led to the establishment of a circumpolar tundra belt and the emergence of temperate grasslands. Most species show a steady population increase during this period, followed by population subdivision during the Last Glacial Maximum about 110,000 to 12,000 years ago. The combination of large effective population sizes and occasional range shifts facilitated contact between the diverging goose species, resulting in high levels of interspecific gene flow. Introgressive hybridization might have enabled these goose populations to quickly adapt to chang- ing environments by transferring of advantageous alleles across species boundaries, increasing standing genetic variation or expanding phenotypic variation of certain traits (e.g., beak morphology). Hybridization seems to be a common and integral com- ponent in the evolution and diversification of geese. The pervasiveness of rapid specia- tion and hybridization in geese complicates the attempt to capture their evolutionary history in a phylogenetic tree, therefore I advocate a phylogenetic network approach. Indeed, trying to capture the complex diversification of the True Geese in a branching tree can be regarded as a wild goose chase. 7 TABLE OF CONTENTS 7 Abstract 11 Chapter 1 – General Introduction: Homage to Saint Martin of Why Are There Still So Many Kinds of Geese? 17 Chapter 2 – Setting the Scene: Species Concepts, Speciation and Hybridization PART I: AVIAN HYBRDIZATION 49 Chapter 3 – The Avian Hybrids Project: Gathering the Scientific Literature on Avian Hybridization 53 Chapter 4 – An Overview of Avian Hybrid Zones and Patterns of Introgression 91 Chapter 5 – Birds in a Bush: Toward an Avian Phylogenetic Network PART II: GOOSE GENOMICS 103 Chapter 6 – Hybridization in Geese: A Review 121 Chapter 7 – A Tree of Geese: A Phylogenomic Perspective on the Evolutionary History of the True Geese 145 Chapter 8 – A History of Hybrids: Genomic Patterns of Introgression in the True Geese 175 Chapter 9 – Synthesis: The Syngameon Scenario and the Exploration of the Adaptive Landscape 199 References 243 Summary 249 Samenvatting 255 Acknowledgements 261 Curriculum Vitae 263 Publications 265 PE&RC training and education statement 268 Colophon Chapter 1 General introduction: homage to Saint Martin or why are there still so many kinds of geese? Chapter 1 1.1 General Introduction The title of this general introduction refers to the classic paper by Hutchinson (1959), Homage to Santa Rosalia or Why Are There So Many Kinds of Animals?, in which he developed an ecological theory to explain species diversity and coexistence. The hom- age to Santa Rosalia refers to the patroness of Palermo, the Italian city where he found inspiration for his theory by observing Water Boatmen (family Corixidae) in a small artificial pond close to a relic for the patroness. The inspiration for this thesis is also based on an observation, namely the occurrence of numerous hybrids between several goose species. How do these goose species coexist and remain distinct despite hybrid- izing? In other words, why are there still so many kinds of geese? In this thesis, the homage refers to Saint Martin of Tours, the patron saint of geese. Hybridization, the interbreeding of different species, has intrigued the earli- est students of natural history. For example, in Historiae Animalium Conrad Gesner (1560) reported several peculiar hybrids, such as the Jumar (an alleged cross between a donkey and a cow). Most of the hybrids described by Gesner (1560) turned out to be fictional, but the interest in hybridization did not diminish (Zirkle, 1935). However, opinions about the importance of hybridization in evolution differed: some regarded hybridization as a creative evolutionary force (Lotsy, 1916, Anderson, 1949, Anderson and Stebbins, 1954, Lewontin and Birch, 1966), while others considered it a byprod- uct of the speciation process (Mayr, 1942, Mayr, 1963, Dobzhansky, 1937, Templeton, 1989). The development of molecular techniques in combination with the study of hybrid zones led to more insights into the dynamics and outcomes of hybridization (Barton and Hewitt, 1985, Moore, 1977). Currently, the significance of hybridization in evolution is acknowledged (Schwenk et al., 2008) as it is involved in several import- ant evolutionary processes. There is a complex interplay between hybridization and speciation (Abbott et al., 2013, Seehausen, 2004): on the one hand, hybridization can slow down or reverse the speciation process (Seehausen, 2006, Seehausen et al., 2008a), while, on the other hand, it can contribute to the completion of speciation by means of reinforcement (Howard, 1993, Servedio and Noor, 2003) and even give rise to new species by hybrid speciation (Mallet, 2007, Mavarez and Linares, 2008, Schumer et al., 2014). In addi- tion, backcrossing of fertile hybrids can amount to the exchange of genetic materi- al between species, a phenomenon known as introgression (Anderson, 1949, Mallet, 2005). Introgressive hybridization can facilitate the interspecific transfer of adaptive 12 General introduction traits (i.e., adaptive introgression; Arnold et al., 2008, Arnold and Martin, 2009, Hed- rick, 2013). Hybridization is mostly rare on a per-individual level, but can be common on a species level (Mallet, 2005). For example, hybrids between European mammals have been recorded for at least 6% of the species (Gray, 1972) and for butterflies the estimates of hybridization incidence range from 6% to 23%, depending on the fami- ly (Mallet, 2005). Grant and Grant (1992) calculated that about 10% of bird species have hybridized with at least one other species. The incidence of hybridization varies among bird orders with Anseriformes (waterfowl: ducks, geese and swans) showing the greatest propensity to hybridize. The study of waterfowl hybridization is biased towards ducks, as exemplified by an extensive inventory of hybrid ducks (Gillham and Gillham, 1998), an analysis of hybrid duck fertility patterns (Tubaro and Lijtmaer, 2002) and various genetic studies on introgressive hybridization (Kraus et al., 2012, Lavretsky et al., 2016, Peters et al., 2014a, McCracken and Wilson, 2011, Joseph et al., 2009). The knowledge on goose hybridization is clearly lagging behind. The True Geese are classified in the waterfowl tribe Anserini (Order Anseri- formes, Family Anatidae, Table 1.1) and have been traditionally divided over two gen- era: Anser and Branta (Delacour and Mayr, 1945). Hybrids have been reported within each genus (Delnicki, 1974, Hatch and Shortt, 1976, Leafloor et al., 2013, Nijman et al., 2010, Trauger et al., 1971, Weckstein et al., 2002), but also intergeneric hybrids have been documented (Craven and Westemeier, 1979, Nelson, 1952, Prevett and Ma- cinnes, 1973). Whether the occurrence of goose hybrids is a recent phenomenon or a common feature during their evolution remains to be investigated. Several studies have reported evidence for ancient hybridization in particular bird groups (McCor- mack and Venkatraman,
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