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Cryptic Speciation in the Warbling Vireo (Vireo Gilvus) Scott F

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Cryptic Speciation in the Warbling Vireo (Vireo Gilvus) Scott F AmericanOrnithology.org Volume 138, 2021, pp. 1–16 DOI: 10.1093/ornithology/ukaa071 RESEARCH ARTICLE Cryptic speciation in the Warbling Vireo (Vireo gilvus) Scott F. Lovell,a,*, M. Ross Lein, and Sean M. Rogers Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada a Current address: Department of Biology, St. Mary’s University, Calgary, Alberta, Canada Downloaded from https://academic.oup.com/auk/article/138/1/ukaa071/6104490 by AOS Member Access user on 03 March 2021 * Corresponding author: [email protected] Submission Date: April 20, 2020; Editorial Acceptance Date: October 8, 2020; Published January 20, 2021 ABSTRACT Eastern (Vireo gilvus gilvus) and western (V. g. swainsoni) forms of the Warbling Vireo have essentially allopatric breeding ranges across north-central North America, but come into contact in central Alberta, Canada. In 1986, Jon Barlow presented preliminary morphological and song evidence suggesting that the Warbling Vireo complex might comprise more than one valid species. However, to date, Barlow’s suggestion is supported by only limited DNA evidence, demonstration of molt and migration differences between the taxa, and anecdotal accounts of differences in song, morphology, plumage, and ecology. We analyzed variation in both mitochondrial and nuclear DNA in birds from Alberta and surrounding areas to determine the levels of genetic differentiation and hybridization occurring in the contact zone, and whether the two taxa warrant recognition as separate biological species. Our analyses reveal that Warbling Vireos in Alberta and the surrounding areas are separated into two well- defined, genetically differentiated, and monophyletic clades corresponding to previously recognized taxonomic groups. The two taxa come into contact in a narrow (~85 km) zone in Barrhead County, northwest of Edmonton, Alberta. They show evidence of limited hybridization. The distinct genetic differences are maintained in the contact zone, where individuals of the two taxa may occupy neighboring territories. Differences in spring arrival dates, molt schedules, and migration routes indicate that a migratory divide may play an important role in reproductive isolation. We suggest that the two taxa are distinct cryptic species: an eastern form, Vireo gilvus, and a western form, Vireo swainsoni. Keywords: hybridization, Pleistocene, reproductive isolation, speciation, Vireo gilvus, Warbling Vireo LAY SUMMARY • Two subspecies of Warbling Vireo meet in a narrow contact zone in central Alberta, Canada. • Analysis of mitochondrial and nuclear DNA found significant genetic differentiation between the two taxa, suggesting a divergence in the early Pleistocene. • Hybrids between the two taxa were uncommon in the contact zone. • These findings suggest that the two taxa are reproductively isolated and, therefore, should be recognized as “good” biological species. Especiación críptica en Vireo gilvus RESUMEN Vireo gilvus presenta dos formas, V. g. gilvus y V. g. swainsoni, que tienen esencialmente rangos reproductivos alopátricos a través del norte y centro de Norteamérica, pero que entran en contacto en el centro de Alberta, Canadá. En 1986, Jon Barlow presentó evidencia preliminar morfológica y de canto sugiriendo que el complejo de V. gilvus podría incluir más de una especie válida. Sin embargo, a la fecha la sugerencia de Barlow está apoyada solo por evidencia limitada de ADN, la demostración de diferencias de muda y migración entre los taxones, y relatos anecdóticos de diferencias en canto, morfología, plumaje y ecología. Analizamos variaciones en ADN mitocondrial y nuclear en las aves de Alberta y las áreas circundantes para determinar los niveles de diferenciación genética e hibridación que se presentan en la zona de contacto, y si los dos taxones justifican el reconocimiento como especies biológicas separadas. Nuestros análisis revelan que V. gilvus en Alberta y las áreas circundantes está separado en dos clados monofiléticos bien definidos, genéticamente diferenciados, correspondiéndose con los grupos taxonómicos previamente reconocidos. Los dos taxones se ponen en contacto en una zona estrecha (~85 km) en el Condado de Barrhead, noroeste de Edmonton, Alberta. Ellos muestran evidencia de hibridación limitada. Las diferencias genéticas distintivas se mantienen en la zona de contacto, donde los individuos de los dos taxones pueden ocupar territorios vecinos. Las diferencias en las fechas de arribo en primavera, en Copyright © American Ornithological Society 2021. All rights reserved. For permissions, e-mail: [email protected]. 2 Warbling Vireo speciation S. F. Lovell, M. R. Lein, and S. M. Rogers los esquemas de muda y en las rutas migratorias indican que una división migratoria puede jugar un rol importante en el aislamiento reproductivo. Sugerimos que los dos taxones son dos especies crípticas distintas: una forma este, Vireo gilvus, y una forma oeste, Vireo swainsoni. Palabras clave: aislamiento reproductivo, especiación, hibridación, Pleistoceno, Vireo gilvus INTRODUCTION 1989). They can persist through evolutionary time (e.g., Arnold 1997, Baxter et al. 1997), or rapidly result in the The climatic cycles of the Pleistocene Epoch (2.6–11 kya) collapse of one or both parental species (e.g., Whitmore had profound influences on the avian biota of temperate 1983, Echelle and Connor 1989). Downloaded from https://academic.oup.com/auk/article/138/1/ukaa071/6104490 by AOS Member Access user on 03 March 2021 North America and Europe (Rand 1948, Johnson and While the scenarios of taxa hybridizing in secondary Cicero 2004, Weir and Schluter 2004, Saitoh et al. 2010). contact zones are well documented in the literature In particular, the ranges of species inhabiting the boreal (Barton and Hewitt 1985, Abbott et al. 2013), the evolu- and montane forests at higher latitudes shifted in location, tionary processes involved, the maintenance of the hybrid and contracted and expanded in response to the repeated zones, the potential outcomes, and the importance of these advance and retreat of continental glaciers. Significantly, zones are still the subjects of much debate (Barton 2013, glacial advances split some wide-ranging species into two Fraïsse et al. 2014, Gompert et al. 2017). or more disjunct populations isolated in separate refugia Hybrid zones often exhibit clines for an array of south of the ice sheets (Hubbard 1973, Weir and Schluter characters that are similar in their location (concordant) 2004, Lovette 2005). Such populations subsequently had and width (coincident), and the transition from one pa- independent evolutionary trajectories while in allopatry, rental taxon to the other is usually abrupt, occurring over potentially developing significant genetic and phenotypic a short distance (Moore 1977). Cline theory (Haldane differences in response to varying selective pressures in 1948, Slatkin 1973, Endler 1977, Barton and Gale 1993) their novel environments and lack of gene flow among provides a conceptual and mathematical framework to populations in different refugia (Pielou 1991, Avise 2000, understand the maintenance of clines and the spread of Weir and Schluter 2004, Toews and Irwin 2008, Irwin traits or genes across hybrid zones (Endler 1977, Barton et al. 2009). 1979, Barton and Hewitt 1985, Barton and Gale 1993). Today, we observe the outcome of range expansions Three main hypotheses have been proposed to explain following the most recent glacial recession (~11,000 yr the maintenance of hybrid zones and the resulting clines. ago). Formerly isolated taxa in secondary contact dem- The neutral diffusion hypothesis (Endler 1977, Barton onstrate various evolutionary outcomes ranging from and Gale 1993) predicts that, in the absence of selection free interbreeding to complete reproductive isolation or a barrier to reproduction, cline width will be propor- (Avise and Walker 1998, Johnson and Cicero 2004, Weir tional to the product of the root-mean-square (RMS) and Schluter 2004, Abbott et al. 2013). These cases pro- dispersal distance per generation and the square root of vide opportunities to examine the processes of evolution, the number of generations since secondary contact. The speciation, selection, and genetic interactions between bounded hybrid superiority hypothesis (Moore 1977, populations (Mayr 1963, Mallet 1995, Coyne and Orr 2004, Moore and Price 1993) states that hybrid zones occur in Price 2008, Abbott et al. 2013). However, uncertainty re- ecotonal areas and are maintained by selection favoring mains regarding the importance of the most recent glacial hybrid individuals and against parental individuals in cycles in generating pairs of divergent populations, relative the hybrid zone. The width of the hybrid zone under this to that of earlier cycles (e.g., Klicka and Zink 1997, Johnson hypothesis is dictated by the width of the ecotone. The and Cicero 2004, Weir and Schluter 2004, Lovette 2005). tension zone or dynamic-equilibrium hypothesis (Barton The impact of the Pleistocene glacial cycles is par- and Hewitt 1985) assumes that hybrids have reduced fit- ticularly noticeable along the Front Range of the Rocky ness, and that a stable hybrid zone persists because the Mountains in Alberta, where the boreal forest meets the reduced fitness of hybrids is balanced by constant move- montane coniferous forest. Numerous pairs of avian taxa ment of “pure” parental taxa into the zone. Therefore, a have secondary contact zones between montane and bo- tension zone exists as a dynamic equilibrium
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