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Admixture Zones in Uganda

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Admixture Zones in Uganda Received: 23 April 2018 | Revised: 26 October 2018 | Accepted: 5 November 2018 DOI: 10.1111/mec.14957 ORIGINAL ARTICLE The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda Norah P. Saarman1 | Robert Opiro2 | Chaz Hyseni3 | Richard Echodu2 | Elizabeth A. Opiyo2 | Kirstin Dion1 | Thomas Johnson1 | Serap Aksoy4 | Adalgisa Caccone1 1Department of Ecology and Evolutionary Biology, Yale University, New Haven, Abstract Connecticut Understanding the mechanisms that enforce, maintain or reverse the process of spe- 2 Department of Biology, Faculty of ciation is an important challenge in evolutionary biology. This study investigates the Science, Gulu University, Uganda patterns of divergence and discusses the processes that form and maintain divergent 3Department of Biology, University of Mississippi, Oxford, Mississippi lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies 4Department of Epidemiology of Microbial from 18 sites spanning known genetic lineages and the four admixture zones be- Diseases, Yale School of Public Health, New Haven, Connecticut tween them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double-digest Correspondence Norah P. Saarman, Department of Ecology restriction site-associated DNA (ddRAD) SNPs to assess genome-wide admixture, 16 and Evolutionary Biology, Yale University, microsatellites to provide continuity with published data and accurate biogeographic New Haven, CT. Email: [email protected] modelling, and a 491-bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions im- Funding information Foundation for the National Institutes pacted by the reorganization of Uganda's river networks that occurred during the of Health, Grant/Award Number: formation of the West African Rift system over the last several hundred thousand 5T32AI007404-24 and AI068932; Fogarty International Center, Grant/Award Number: years. Because tsetse fly population distributions are defined by rivers, admixture D43TW0 zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together. KEYWORDS ddRAD, hybridization, population genomics, speciation, trypanosomiasis, vector 1 | INTRODUCTION 2004), periods of potential gene flow (secondary contact) are also common during speciation (Davison, Chiba, Barton, & Clarke, Genetic divergence occurs when the forces of mutation, genetic 2005; Martin, Dasmahapatra, Nadeau, Salazar, & Walters, 2013). drift and local adaptation cause differences in genotype frequen- Secondary contact can alter the evolutionary trajectory of the cies between isolated populations. Although divergence occurs divergent lineages by enforcing, maintaining or even reversing most often during periods of geographic isolation (Coyne & Orr, divergence (Barton, 2001; Grant & Grant, 2008) by a balance 66 | © 2018 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/mec Molecular Ecology. 2019;28:66–85. SAARMAN ET AL. | 67 between gene flow and the strength of selection against hy- term “admixture zones” instead of “hybrid zones” in the context of brids (Barton & Bengtsson, 1986; Barton & Hewitt, 1985; Collins this system because it is not clear whether they represent regions & Rawlins, 2013; Mullen, Dopman, & Harrison, 2008; Turelli, of secondary contact between reproductively isolated lineages. Barton, & Coyne, 2001). The ecological and evolutionary pro- Instead, admixture zones could be regions undergoing primary di- cesses underlying this balance appear to be contingent on the vergence with gene flow or they could represent the remnants of environmental, demographic and genomic context of secondary old collapsed hybrid zones (e.g., in North American ravens, Webb, contact (reviewed in Gompert, Mandeville, & Buerkle, 2017) and Marzluff, & Omland, 2011; in Galapagos giant tortoises, Garrick et remain an important question in speciation research and popula- al., 2014; in Galapagos finches, Grant & Grant, 2006). tion genetics in general. Patterns of hybridization and introgres- The multiple admixture zones in this system provide an oppor- sion (gene flow among divergent lineages) across such regions of tunity to compare the genetic structure, biogeographic context, secondary contact provide an opportunity to elucidate the eco- and patterns of hybridization and introgression among them. One logical and evolutionary processes important in divergence. expectation established in the hybrid zone literature is that the Tsetse flies (genus Glossina) are a promising system to inves- context-dependent nature of reproductive isolation can create tigate secondary contact because of their extensive population an array of introgression patterns in multiple hybrid zones (Coyne structure and evidence of admixture. The species Glossina fusci‐ & Orr, 2004; Gompert et al., 2017), even within the same system pes fuscipes is particularly well-suited for this line of questioning (Bierne, Bonhomme, & David, 2003). Understanding introgression because there is evidence of admixture across multiple genetic patterns can shed light on the evolutionary and ecological processes breaks representing different stages of divergence (Beadell et important in the process of speciation. For example, a long-stand- al., 2010; Echodu et al., 2013; Opiro et al., 2017). Furthermore, ing question in speciation research is the relative importance of al- G. f. fuscipes offers the advantage of being the object of intense ternative forms of postzygotic reproductive barriers (i.e., intrinsic applied research in population structure, ecology, genetics and Dobzhansky–Muller incompatibilities vs. extrinsic ecological barri- physiology because of their epidemiological relevance as the ers: Barton, 2001, Schluter, 2000; Coyne & Orr, 2004; Funk, Nosil, & obligate vectors of animal and human African trypanosomiasis Etges, 2006; Gompert et al., 2017; Gross & Rieseberg, 2005; Rundle (Aksoy, Caccone, Galvani, & Okedi, 2013; Kleine, 1909; Riley & & Nosil, 2005). Recent theoretical work suggests that extrinsic and Johannsen, 1932). intrinsic barriers may not work in isolation, but instead can work Previous research described four genetic clusters of G. f. fusci‐ synergistically in zones of secondary contact (i.e., the “coupling hy- pes centred in the northwest, northeast, west and south of the pothesis”; Bierne, Welch, Loire, Bonhomme, & David, 2011). Under country, with evidence of admixture between these clusters a model of divergence with gene flow, the coupling of multifarious (Figure 1; Beadell et al., 2010; Opiro et al., 2017). We use the barriers can rapidly advance the process of speciation from early to Northwest (NW) AFRICA 3 Achwa 2 River FIGURE 1 Map of Uganda and the 4 1 location of the 18 sampling sites of Albert Nile Glossina fuscipes fuscipes used in this “b” study. Each sampling site marker indicates Species range “a” Okole its placement relative to the distribution Lakes River 6 5 Waterways of the four pure genetic backgrounds 13 9 7 Admixture West 8 (northwest: shaded pink, northeast: Murchison Falls Northeast (W) 10 shaded blue, west: shaded green, south: 11 (NE) Site Codes 14 shaded orange), and is color-coded by Lake Kafu 01-DUK (NW) Albert River 15 Lake the watershed it falls within (Albert Nile: Kyoga 02-ORB (NW) 16 pink, Achwa River: magenta, Okole River: 03-NGO (NW) “c” 04-BOL (“b”) purple, Lake Kyoga: blue, Lake Albert: 05-CHU (“b”) “d” light green, Kafu River: dark green, Lake 06-ACA (“b”) 12 07-APU (“b”) Lake Victoria: orange). The species distribution 08-OCA (“b”) 18 17 South (S) Victoria of G. f. fuscipes beyond the distribution 09-UWA (“a”) UGANDA 10-OCU (NE) of the four pure genetic backgrounds is 11-OT (NE) shown in light grey, and admixture zones 12-BN (“d”) 13-MF (W) (“a”, “b”, “c” and “d”) within this shading 14-MS (W) are indicated with arrows pointing to 15-KAF (“c”) 16-JN (“c”) the genetic backgrounds in putative 17-NB (“d”) secondary contact in each zone. [Colour 18-WAM (S) 50 050100 150200 km figure can be viewed at wileyonlinelibrary. com] 68 | SAARMAN ET AL. late stages (Gompert et al., 2017). One prediction of this hypothesis in shaping genetic structure observed (Beadell et al., 2010; Hyseni is the rare occurrence of stable long-lasting hybrid zones (Gompert et al., 2012; Opiro et al., 2017). To capture this geographic aspect, et al., 2017), which implies rarity of first-generation hybrids as well as sampling was distributed across the seven major watersheds, and intermediate levels of introgression in nature. Here, we investigate all descriptive analysis (i.e., genetic diversity, heterozygosity and this prediction with a comparison of introgression patterns found in structure) used the natural boundaries created by the watersheds G. f. fuscipes, a unique system with four admixture zones that exist (Figure 1, Table 1). We chose to define groups for descriptive anal- within
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