Hidden endemism, deep polyphyly, and repeated dispersal across the Isthmus of Tehuantepec: Diversification of the White‐collared Seedeater complex (Thraupidae: Sporophila torqueola)

Abstract

Phenotypic and genetic variation are present in all species, but lineages differ in how variation is partitioned among populations. Examining phenotypic clustering and genetic structure within a phylogeographic framework can clarify which biological processes have contributed to extant biodiversity in a given lineage. Here, we investigate genetic and phenotypic variation among populations and subspecies within a Neotropical songbird complex, the White‐collared Seedeater (Sporophila torqueola) of Central America and Mexico. We combine measurements of morphology and plumage patterning with thousands of nuclear loci derived from ultraconserved elements (UCEs) and mitochondrial DNA to evaluate population differentiation. We find deep levels of molecular divergence between two S. torqueola lineages that are phenotypically diagnosable: One corresponds to S. t. torqueola along the Pacific coast of Mexico, and the other includes S. t. morelleti and S. t. sharpei from the Gulf Coast of Mexico and Central America. Surprisingly, these two lineages are strongly differentiated in both nuclear and mitochondrial markers, and each is more closely related to other Sporophila species than to one another. We infer low levels of gene flow between these two groups based on demographic models, suggesting multiple independent evolutionary lineages within S. torqueola have been obscured by coarse‐scale similarity in plumage patterning. These findings improve our understanding of the biogeographic history of this lineage, which includes multiple dispersal events out of South America and across the Isthmus of Tehuantepec into Mesoamerica. Finally, the phenotypic and genetic distinctiveness of the range‐restricted S. t. torqueola highlights the Pacific Coast of Mexico as an important region of endemism and conservation priority.

Aves del Alto Balsas de Guerrero: diversidad e identidad ecológica de una región prioritaria para la conservación

“…En cuanto a endemismos e identidad biológica mexicana, la riqueza de especies endémicas registrada hace del Alto Balsas un área prioritaria para la conservación a escala global (Arizmendi, 2002;Bertelli et al, 2017; Navarro-Sigüenza y Peterson, 2004;Peterson y Navarro-Sigüenza, 2000). En términos históricos, la evolución de endemismos en los bosques tropicales secos del occidente de México se explica por varios factores: el efecto de aislamiento que la Faja Volcánica Transmexicana y la sierra Madre del Sur producen sobre la cuenca del Balsas (Becerra, 2005;Morrone, 2014); el levantamiento del istmo de Tehuantepec durante el Mioceno (Mason et al, 2018;Navarro-Sigüenza et al, 2017) y los cambios paleoclimáticos derivados del avance y retroceso de glaciares del Pleistoceno (Arbeláez-Cortés, Milá et al, 2014;Arbeláez-Cortés, Roldán-Piña et al, 2014;Montaño-Rendón et al, 2015;Navarro-Sigüenza et al, 2017). En conjunto, estos procesos moldearon la distribución de los bosques templados y tropicales, generando efectos de aislamiento y contacto periódicos que elevaron las tasas de diversificación de las aves (Lovette, 2005).…”

“…Por esta razón, se le considera un área de endemismo de aves de importancia global (EBA-008; Stattersfield et al, 1999). Este patrón se origina por el aislamiento orográfico de la cuenca (Morrone, 2014), los cambios paleoecológicos que moldearon la cobertura de bosques tropicales y templados, provocando efectos de aislamiento y diversificación de especies restringuidas entre final del Mioceno (Mason et al, 2018;Navarro-Sigüenza et al, 2017) y el Pleistoceno (Linares-Palomino et al, 2011;Lovette, 2005;Pennington et al, 2000). Por esta conjugación de factores ecológicos e históricos, la avifauna de la cuenca del Balsas posee un gran valor para la biodiversidad mexicana (Espinosa-Organista et al, 2008;Morrone, 2014;Ríos-Muñoz, 2013).…”

Peer Review #2 of "Ultraconserved elements (UCEs) illuminate the population genomics of a recent, high-latitude avian speciation event (v0.1)"

“…Although UCEs are highly conserved at their core, which enables universal capture of loci across diverse groups of organisms (Faircloth et al 2012(Faircloth et al , 2013(Faircloth et al , 2015Starret et al 2016), lower levels of purifying selection away from the core allow substitutions to accumulate in the flanking regions. Using human genome data, Faircloth et al (2012) demonstrated that the increased variation in UCE flanking sequence might be adequate to make these loci useful for questions at shallow levels of divergence, and this hypothesis has been supported by subsequent empirical studies (Smith et al 2014, Harvey & Brumfield 2015, Oswald et al 2016, Mason et al 2018. However, the utility of UCE loci for studying population genetics, population divergence, and/or incipient speciation is only beginning to be tested, and both the value and challenges of using UCEs at these shallow levels remain underexplored.…”

“…Outside of their functional relevance, UCE loci have demonstrated utility for recovering deeperlevel phylogenetic relationships (McCormack et al 2013, Faircloth et al 2015, Gilbert et al 2015) and shallower-level genus and population relationships (Smith et al 2014, Harvey & Brumfield 2015, Leaché et al 2015, Manthey et al 2016, Oswald et al 2016, Mason et al 2018. Although UCEs are highly conserved at their core, which enables universal capture of loci across diverse groups of organisms (Faircloth et al 2012(Faircloth et al , 2013(Faircloth et al , 2015Starret et al 2016), lower levels of purifying selection away from the core allow substitutions to accumulate in the flanking regions.…”

Ultraconserved elements (UCEs) illuminate the population genomics of a recent, high-latitude avian speciation event

“…Outside of their functional relevance, UCE loci have demonstrated utility for recovering deeperlevel phylogenetic relationships (McCormack et al 2013, Gilbert et al 2015) and shallower-level genus and population relationships (Smith et al 2014, Harvey & Brumfield 2015, Leaché et al 2015, Manthey et al 2016, Oswald et al 2016, Mason et al 2018. Although UCEs are highly conserved at their core, which enables universal capture of loci across diverse groups of organisms (Faircloth et al 2012(Faircloth et al , 2013(Faircloth et al , 2015Starret et al 2016), lower levels of purifying selection away from the core allow substitutions to accumulate in the flanking regions.…”