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Biodiversity Genomics of North American Dryobates Woodpeckers

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Biodiversity Genomics of North American Dryobates Woodpeckers applyparastyle "fig//caption/p[1]" parastyle "FigCapt" AmericanOrnithology.org Volume XX, 2019, pp. 1–12 DOI: 10.1093/auk/ukz015 RESEARCH ARTICLE Biodiversity genomics of North American Dryobates woodpeckers reveals Downloaded from https://academic.oup.com/auk/advance-article-abstract/doi/10.1093/auk/ukz015/5454745 by New York University user on 28 April 2019 HeadA=HeadB=HeadA=HeadB/HeadA little gene flow across the D. nuttallii x D. scalaris contact zone HeadB=HeadC=HeadB=HeadC/HeadB Extract2=HeadB=Extract=HeadB Joseph D. Manthey,1,2,3,*, Stéphane Boissinot,2 and Robert G. Moyle3 Extract2=HeadA=Extract=HeadA 1 Extract3=HeadA=Extract1=HeadA Department of Biological Sciences, Texas Tech University, Lubbock, Texas, USA 2New York University Abu Dhabi, Abu Dhabi, UAE Extract3=HeadB=Extract1=HeadB 3Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, USA HeadA=HeadB=HeadA=HeadB/HeadA *Corresponding author: [email protected] HeadB=HeadC=HeadB=HeadC/HeadB Submission Date: September 7, 2018; Editorial Acceptance Date: February 1, 2019; Published April 13, 2019 HeadC=HeadD=HeadC=HeadD/HeadC Extract3=HeadA=Extract1=HeadA REV_HeadA=REV_HeadB=REV_HeadA=REV_HeadB/HeadA ABSTRACT Evolutionary biologists have long used behavioral, ecological, and genetic data from contact zones between closely REV_HeadB=REV_HeadC=REV_HeadB=REV_HeadC/HeadB related species to study various phases of the speciation continuum. North America has several concentrations of REV_HeadC=REV_HeadD=REV_HeadC=REV_HeadD/HeadC avian contact zones, where multiple pairs of sister lineages meet, with or without hybridization. In a southern California REV_Extract3=REV_HeadA=REV_Extract1=REV_HeadA contact zone, 2 species of woodpeckers, Nuttall’s Woodpecker (Dryobates nuttallii) and the Ladder-backed Woodpecker EDI_HeadA=EDI_HeadB=EDI_HeadA=EDI_HeadB/HeadA (D. scalaris), occasionally hybridize. We sampled these 2 species in a transect across this contact zone and included EDI_HeadB=EDI_HeadC=EDI_HeadB=EDI_HeadC/HeadB samples of their closest relative, the Downy Woodpecker (D. pubescens), to obtain large single nucleotide polymorphism EDI_HeadC=EDI_HeadD=EDI_HeadC=EDI_HeadD/HeadC panels using restriction-site associated DNA sequencing (RAD-seq). Furthermore, we used whole-genome resequencing EDI_Extract3=EDI_HeadA=EDI_Extract1=EDI_HeadA data for 2 individuals per species to identify whether patterns of diversity inferred from RAD-seq were representative of whole-genome diversity. We found that these 3 woodpecker species are genomically distinct. Although low levels CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA of gene flow occur between D. nuttallii and D. scalaris across the contact zone, there was no evidence for widespread CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB genomic introgression between these 2 species. Overall patterns of genomic diversity from the RAD-seq and whole- CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC genome datasets appear to be related to distributional range size and, by extension, are likely related to effective CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA population sizes for each species. ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA Keywords: contact zone, Dryobates, genomics, hybrid zone, Picoides, RAD-seq, woodpeckers ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC La biodiversidad genómica de los carpinteros Dryobates de América del Norte revela poco flujo génico a Keywords=HeadA=Keywords=HeadA_First través de la zona de contacto de D. nuttallii x D. scalaris CORI_Text_First=CORI_Text=CORI_Text_First=CORI_TextInd RESUMEN Box_Head=Box_AHead=Box_Head=Box_AHead/Head Los biólogos evolutivos han usado durante mucho tiempo datos comportamentales, ecológicos y genéticos de las zonas de contacto entre especies cercanamente emparentadas para estudiar varias fases del proceso continuo de especiación. América del Norte tiene varias concentraciones de zonas de contacto de aves, dónde múltiples pares de linajes hermanos se encuentran, con o sin hibridación. En una zona de contacto del sur de California, dos especies de carpinteros, Dryobates nuttallii y D. scalaris, hibridan ocasionalmente. Muestreamos estas dos especies en un transecto a través de esta zona de contacto e incluimos muestras de su pariente más cercano, D. pubescens, para obtener grandes paneles de polimorfismo de un solo nucleótido (SNP) usando secuenciación de sitios de restricción asociados al ADN (RAD-seq por sus siglas en inglés). Además, usamos datos de re-secuenciación de todo el genoma para dos individuos por especie, para identificar si los patrones de diversidad inferidos a partir de RAD-seq fueron representativos de toda la diversidad genómica. Encontramos que estas tres especies de carpinteros son genómicamente distintas. Aunque existen bajos niveles de flujo génico entre D. nuttallii y D. scalaris a través de la zona de contacto, no hubo evidencia de una amplia introgresión genómica entre estas dos especies. Los patrones generales de diversidad genética a partir de RAD-seq y los datos del genoma completo parecen estar relacionadas con el tamaño del rango de distribución, y por extensión, están probablemente relacionadas con los tamaños poblacionales efectivos para cada especie. Palabras clave: carpinteros, Dryobates, genómica, Picoides, RAD-seq, zona de contacto, zona híbrida INTRODUCTION ecosystems in continental North America, as well as tran- sitions between ecosystems, has resulted in a plethora of Contact zones, where species may or may not hybridize, are closely related species complexes with partially overlap- ideal locations to study the effects of barriers to gene flow ping distributions (i.e. contact zones; Remington 1968). and introgression on the process of speciation between With geographic contact between closely related species closely related species (Hewitt 1988). The multitude of comes the opportunity for gene flow and introgression Copyright ©American Ornithological Society 2019. All rights reserved. For permissions, e-mail: [email protected]. 2 Dryobates biodiversity genomics J. D. Manthey, S. Boissinot, and R. G. Moyle across species boundaries. In North American birds, these Nuttall’s Woodpecker (D. nuttallii) (Figure 1A, B). D. sca- contact zones are concentrated in the Great Plains, the laris and D. nuttallii are known to occasionally hybridize transition between the Rocky Mountains and Cascade in southern California, USA, and Northern Baja California, Mountains, and in the sky islands of southwestern USA Mexico (Short 1971) (Figure 1), although they do not have and northwestern Mexico (Remington 1968, Rising 1983, a broad or well-documented hybrid zone. Downloaded from https://academic.oup.com/auk/advance-article-abstract/doi/10.1093/auk/ukz015/5454745 by New York University user on 28 April 2019 Swenson and Howard 2005). D. nuttallii and D. scalaris are distinguishable by In some North American regions, hybridization is fre- slight differences in morphology and plumage, including quent between closely related but morphologically di- bill length and patterning of black and white feathers on vergent species, resulting in gene flow across species head, back, and rectrices (Short 1971). Additionally, hab- boundaries, as documented in buntings (Passerina), and itat preferences and vocalizations differ between these grosbeaks (Pheucticus) (Carling and Brumfield 2008, sister species; D. nuttallii and D. scalaris differ in their Mettler and Spellman 2009). In contrast, hybridization calls and drumming (Winkler and Short 1978, Stark et al. in other North American birds may be infrequent—indi- 1998), and D. nuttallii inhabits oak and riparian forests in cated by the detection of little gene flow or introgression California (Figure 1A), whereas D. scalaris inhabits dry between lineages— as is seen in treecreepers (Certhia) and stunted forest, scrub, and desert across southwestern USA wood-pewees (Contopus), despite general morphological and northwestern Mexico (Figure 1A). The distinct habitat similarity between sister taxa (Manthey and Robbins 2016, preferences and song divergence of D. nuttallii and D. sca- Manthey et al. 2016). In cases of limited gene flow between laris likely limit their opportunities for hybridization and closely related phenotypically similar taxa, behavioral rec- subsequent introgression between the species; they come ognition (e.g., song) and ecological preferences or adapta- into contact in areas where the lower elevation oak forest tions are potential pre-mating isolation mechanisms rather or riparian forest meets drier habitat, such as Joshua tree than visual recognition (Slabbekoorn and Smith 2002). In (Yucca brevifolia) forest abutting riverine areas. Because of these systems, hybridization is physically possible but in- these distinct habitat differences, the contact zone between frequent, and leads to the question: Does infrequent hy- these 2 Dryobates woodpeckers occurs in a geographic re- bridization influence genomic distinctiveness of sister gion lacking other North American avian contact zones species? (Remington 1968, Swenson and Howard 2005). Several North American woodpeckers (Picidae, genera: Regardless of their differences, D. nuttallii x D. scalaris Colaptes, Dryobates, Melanerpes, and Sphyrapicus) have hybrids have been identified in multiple contexts. Short contact zones with varying levels of hybridization: from a (1971) studied the morphology of hundreds of D. nuttallii broad
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