Habitat connectivity, gene flow, and population genetic structure in a Neotropical understory insectivore, the Rufous-and-white Wren

AmericanOrnithology.org Volume 139, 2022, pp. 1–14 https://doi.org/10.1093/ornithology/ukac030 RESEARCH ARTICLE Habitat connectivity, gene flow, and population genetic structure in a Neotropical understory insectivore, the Rufous-and-white Wren Brendan A. Graham,1,2,a,*, Daniel D. Heath,1,3 Paulo C. Pulgarin,4 Ryan P. Walter,5 Melissa Mark,6 and Daniel J. Mennill1, Department of Integrative Biology, University of Windsor, Windsor, Ontario, Canada Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, Canada 3 Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, Canada 4 Neotropical Ornithological Society, Medellín, Columbia 5 Biological Science, California State University, Fullerton, California, USA 6 Doris Duke Conservation Scholars Program, University of Washington, Seattle, Washington, USA a Current address: Institute of Arctic Biology, University of Fairbanks, Fairbanks, AK, USA *Corresponding author: 1 2 ABSTRACT Among tropical organisms, heightened habitat specialization, limited natal dispersal, and strong philopatry suggest that many species may experience reduced rates of gene flow. Diverse forms of barriers, including geographic, ecological, and behavioral barriers, further promote genetic divergence among tropical bird populations. Here, we extend our comprehension of gene flow in tropical birds by examining population genetic structure in a widespread insectivorous songbird of the Neotropics, the Rufous-and-white Wren (Thryophilus rufalbus). We explore the effects of geographic distance and habitat connectivity on genetic structure using 10 microsatellite loci, and nuclear and mitochondrial sequence data. We report high levels of genetic divergence and population structure with reduced contemporary gene flow between populations over a 500-km transect in Nicaragua and Costa Rica. Mitochondrial DNA and nuclear sequence data indicate that 2 distinct mtDNA genetic groups came into contact in northwestern Costa Rica; molecular dating suggests that the genetic patterns arose as a result of Pleistocene glaciations. Geographic distance and habitat connectivity predicted genetic structure but explained a relatively low proportion of the observed contemporary genetic variation. Patterns were similar for both males and females. Our research demonstrates the deep genetic divergence in tropical birds, and that genetic differentiation can occur over a relatively short distance. For tropical birds, strong limits to gene flow likely arise as a result of limited dispersal from natal populations. Keywords: gene flow, Neotropics, philopatry, Rufous-and-white Wren, Thryophilus rufalbus, Thryothorus rufalbus LAY SUMMARY • Among tropical organisms, heightened habitat specialization and strong philopatry suggest that many species may experience reduced rates of gene flow. • We explored the effects of geographic distance and habitat connectivity on genetic structure for Rufous-and-white Wrens (Thryophilus rufalbus) using 10 microsatellite loci and nuclear and mitochondrial sequence data. • We observed high levels of population genetic structure and low levels of contemporary gene flow among five populations in Nicaragua and Costa Rica. • We found two distinct genetic clades present in this region, and divergence times suggest that these clades diverged during the last Pleistocene glaciation. • Our research demonstrates the deep genetic divergence in tropical organisms, and that genetic differentiation can occur over a relatively short distance; strong limits to gene flow likely arise as a result of strong philopatry. Conectividad de hábitat, flujo génico y estructura genética poblacional en un insectívoro neotropical de sotobosque, Thryophilus rufalbus RESUMEN Entre los organismos tropicales, la elevada especialización de hábitat, la limitada dispersión natal y la fuerte filopatría sugieren que muchas especies pueden experimentar tasas reducidas de flujo génico. Diversas formas de barreras, Copyright © American Ornithological Society 2022. All rights reserved. For permissions, e-mail: . Submission Date: November 3, 2021; Editorial Acceptance Date: June 21, 2022; Published July 8, 2022 2 Population genetic structure in Rufous-and-white Wrens B. A. Graham et al. Palabras clave: filopatría, flujo génico, Neotrópico, Thryophilus rufalbus INTRODUCTION Biodiversity is highest in the tropics, yet diversity remains underestimated because many regions are poorly sampled and many species have not been studied in detail (Redford et al. 1990, Hebert et al. 2004, Lohman et al. 2010, Bálint et al. 2011). Many tropical species exhibit high population genetic structure across geographic space, characterized by deep genetic divergence observed within species complexes (Cadena and Cuervo 2009, Derryberry et al. 2011, González et al. 2011, Isler et al. 2012, Habel et al. 2013, Lougheed et al. 2013, De Camargo et al. 2015, Céspedes et al. 2021, Del-Rio et al. 2021). The observed genetic patterns are often attributed to the genetic legacy of the Pleistocene (Hewitt 2000, Dhorta et al. 2011, Cabanne et al. 2016), or biogeographic barriers (Burney and Brumfield 2009, Huntley and Voelker 2016, Del-Rio et al. 2021), although anthropogenic alterations to habitat, and outright loss of habitat, also influence genetic patterns (Bates 2002, Athrey et al. 2012, Woltmann et al. 2012a, Barr et al. 2015). Examining patterns of gene flow across diverse landscapes provides important insight into the connectivity of habitats, animal movements, and biodiversity. Tropical birds occupy diverse habitats and often exhibit strong philopatry and niche specialization compared with their temperate counterparts (Russell et al. 2004). Both philopatry and habitat specialization are thought to promote genetic divergence and reduce gene flow between populations and are understood to be important aspects of speciation for birds (Arguedas and Parker 2000, Salisbury et al. 2012, Smith et al. 2014, Peterson et al. 2015, Khimoun et al. 2016). It is widely understood that avian diversity peaks near the equator, but recent research, using the ecological species concept, suggests that avian diversity is severely underestimated (estimates using molecular tools suggest that the number of bird species may be two to two-and-a-half times greater than currently recognized; Barrowclough et al. 2016). In conjunction with the recent description of new species from the Neotropics (e.g., Lara Ornithology 139:1–14 © 2022 American Ornithological Society et al. 2012, Seeholzer et al. 2012, Sandoval et al. 2014, 2017), these findings demonstrate the importance of examining population genetic patterns for tropical birds and can help to guide efforts that conserve tropical biodiversity. In the current study, we focused on Rufous-and-white Wrens (Thryophilus rufalbus), a nonmigratory, understory insectivore with a widespread distribution in the Neotropics. The range of (...truncated)