Phylogeography of the widespread white-eared hummingbird (Hylocharis leucotis): pre-glacial expansion and genetic differentiation of populations separated by the Isthmus of Tehuantepec

Abstract

The Pleistocene glacial cycles had a strong influence on the demography and genetic structure of many species, particularly on northern-latitude taxa. Here we studied the phylogeography of the white-eared hummingbird (Hylocharis leucotis), a widely distributed species of the highlands of Mexico and Central America. Analysis of mitochondrial DNA (mtDNA) sequences was combined with ecological niche modelling (ENM) to infer the demographic and population differentiation scenarios under present and past conditions. Analyses of 108 samples from 11 geographic locations revealed population structure and genetic differentiation among populations separated by the Isthmus of Tehuantepec (IT) and the Motagua-Polochic-Jocotán (MPJ) fault barriers. ENM predicted a widespread distribution of suitable habitat for H. leucotis since the Last Inter Glacial (LIG), but this habitat noticeably contracted and fragmented at the IT. Models for historical dispersal corridors based on population genetics data and ENM revealed the existence of corridors among populations west of the IT; however, the connectivity of populations across the IT has changed little since the LIG. The shallow geographic structure on either side of the isthmus and a star-like haplotype network, combined with the long-term persistence of populations across time based on genetic data and potential dispersal routes, support a scenario of divergence with migration and subsequent isolation and differentiation in Chiapas and south of the MPJ fault. Our findings corroborate the profound effects of Pleistocene climatic fluctuations on the evolutionary history of montane taxa but challenge the generality of expanded suitable habitat (pine-oak forests) during glacial cycles.

Estimation of species divergence times in presence of cross-species gene flow

“…Episodic gene flow between species after they have diverged (introgression) is also known to affect species divergence times but is perhaps less well understood than ILS. Advances in statistical tests for introgression ( Green et al 2010 ; Pease and Hahn 2015 ; Blischak et al 2018 ; Ji et al 2022 ) and phylogenetic network estimation ( Solís-Lemus and Ané 2016 ; Wen et al 2016 ; Zhang et al 2018a ) coupled with contemporary phylogenomic datasets have characterized signals of introgression in many non-model groups across mammals ( Nilsson et al 2018 ; Poelstra et al 2021 ), insects ( Edelman et al 2019 ; Hundsdoerfer et al 2019 ), birds ( Oswald et al 2019 ; Zamudio-Beltran et al 2020 ), and squamates ( Schield et al 2017 ; Barley et al 2019 ). Introgression is especially common in plants—which are notorious for allopolyploid speciation ( Barker et al 2016 )—both within genera ( Crowl et al 2017 ; Wu et al 2018 ; Karimi et al 2020 ) and at deeper phylogenetic levels ( Stull et al 2020 ; Morales-Briones et al 2021 ).…”

Genetic Consequences of Forest Fragmentation in a Widespread Forest Bat (Natalus mexicanus, Chiroptera: Natalidae)

“…In addition, the highest levels of historical gene flow were recorded from PYUC to SS, which could be a reflection of a historical dispersal route through the Isthmus of Tehuantepec, as has been documented in birds [96,97]. The separation between GM/PM and PYUC probably results from the influence of the Isthmus of Tehuantepec, which has functioned as a geographic barrier for flying organisms such as bats [50,51,98] and birds [99,100]; this hypothesis was supported by the moderate gene flow values obtained here. For the group PYUC, signatures of demographic stability over time were observed, a finding also supported by paleontological information; these observations suggest that the general climate of the region did not change drastically from the end of the Pleistocene to the present [101,102].…”

Recent genetic, phenetic and ecological divergence across the Mesoamerican highlands: a study case with Diglossa baritula (Aves: Thraupidae)

“…This timing confirms again that the genetic divergence found here is a consequence of Pleistocene climatic oscillations, and not the emergence of the IT. The IT has played the role of an important geographic barrier in southern Mexico shaping the Mesoamerican highlands biodiversity, in birds ( Pérez-Emán, 2005 ; Barber & Klicka, 2010 ; Zamudio-Beltrán et al, 2020 ) as well as other taxa such as reptiles ( Bryson et al, 2011 ), mammals ( León-Paniagua et al, 2007 ) and plants ( Hernández-Langford, Siqueiros-Delgado & Ruíz-Sánchez, 2020 ).…”