Phylogenomics of arboreal alligator lizards shed light on the geographical diversification of cloud forest‐adapted biotas

Abstract

Aim The proximate ecological and evolutionary processes underlying the high biodiversity of neotropical montane cloud forests are still very poorly understood. Climatic oscillations may have contributed to vicariance and cladogenesis, but also promoted secondary contact and erosion of genetic divergence. Here we tested whether geographical diversification – or its lack thereof – in a complex of arboreal alligator lizards is explained by range shifts during Quaternary climatic oscillations. Location Pine–oak and cloud forests, central Mexico. Taxon Abronia taeniata–graminea species complex (Squamata: Anguidae: Gerrhonotinae). Methods We generated genomic data (ddRADseq) to infer patterns of geographical diversification in the complex, reconstruct its demographic history, estimate the timing of lineage split, and test for the presence of contemporary and/or historical hybridization. We evaluated whether the tempo and mode of diversification (i.e. strict isolation vs. secondary contact with introgression) are explained by the contemporary distribution of suitable habitats and/or range shifts experienced by the complex since the Last Glacial Maximum (LGM), as inferred from environmental niche modelling (ENM). Results Genomic data supported a marked genetic structure within the complex, and phylogenomic and dating analyses revealed cryptic lineage diversification starting at the onset of the Pleistocene followed by secondary contact with limited introgression. ENM pointed to considerable range expansions of the complex during the LGM and a marked fragmentation and scarce connectivity among contemporary populations, which was supported by genomic‐based demographic reconstructions. Main Conclusions The geographical diversification of the complex has been moulded by vicariant events promoted by Pleistocene geologic and climatic changes impacting the distribution of their pine–oak and cloud forest habitats. Our data supported a model of divergence with introgression, indicating that pulses of population fragmentation and expansion during the Quaternary have led to multiple opportunities for both allopatric isolation and secondary contact.

Demographic and spatially explicit landscape genomic analyses in a tropical oak reveal the impacts of late Quaternary climate change on Andean montane forests

“…Our study revealed an important role of landscape heterogeneity and restricted dispersal through unsuitable habitats in determining the marked genetic fragmentation of montane oak forests in the Andean Cordilleras, rejecting the hypothesis of persistent connectivity proposed in previous studies (Zorrilla‐Azcué et al, 2021). Our genomic data support that elevational displacements and corresponding pulses of population merging and fragmentation at local to regional scales were not sufficient to erode the genetic structure of present‐day oak populations and, on the contrary, probably contributed to fuel their geographical diversification (e.g., Gutiérrez‐Rodríguez et al, 2022; Nevado et al, 2018). Future genomic‐based demographic reconstructions for a representative number of taxa of the different vegetation belts in a comparative framework might help to gain further insights into the dynamics of Andean biotas in response to Quaternary climatic oscillations (e.g., see Helmstetter et al, 2020 for a forest community in tropical Africa).…”

“…Our genomic data support that elevational displacements and corresponding pulses of population merging and fragmentation at local to regional scales were not sufficient to erode the genetic structure of present-day oak populations and, on the contrary, probably contributed to fuel their geographical diversification (e.g., Gutiérrez-Rodríguez et al, 2022;Nevado et al, 2018) Flantua et al, 2019;Ornelas et al, 2019;Ramírez-Barahona & Eguiarte, 2013), which is still very limited compared to the welldocumented glacial-interglacial dynamics experienced by temperate biotas (Hewitt, 2004;Stewart et al, 2010). Ongoing biogeographical research in the tropical Andes guarantees future opportunities to further study the consequences of Quaternary climate change in this biodiversity hotspot (e.g., Flantua et al, 2019;Hazzi et al, 2018;Muñoz-Ortiz et al, 2015;Nevado et al, 2018;Sanín et al, 2022) and to gain further insights into the proximate ecological and evolutionary processes that have contributed to its extraordinary levels of endemism (Kier et al, 2009;Myers et al, 2000).…”

Bridging the gap: A new species of arboreal Abronia (Squamata: Anguidae) from the Northern Highlands of Chiapas, Mexico

“…Hypothesized causes of this diversity remain poorly tested, but interrelated biological, geological, and climatic factors are likely at play [5,6]. Many authors generally agree that complex historical processes of mountain formation, together with paleoclimatic events, created biogeographic barriers correlated with speciation in many Middle American vertebrates [7][8][9][10][11][12][13]. Today, striking and emblematic species of birds [14,15], snakes [16,17], frogs [18,19] and salamanders [20,21] live in these mountain woodlands and nowhere else.…”

An elevational shift facilitated the Mesoamerican diversification of Azure‐hooded Jays (Cyanolyca cucullata) during the Great American Biotic Interchange

“…The mechanisms underlying the generation of biodiversity in this region have been the subject of numerous investigations (Bryson et al, 2011 ; DeRaad, Applewhite, et al, 2023 ; Mastretta‐Yanes et al, 2015 ; Ornelas et al, 2010 ; Sullivan et al, 2000 ; Venkatraman et al, 2019 ; Zarza et al, 2016 ). While vicariance seems to have played a major role in speciation—whether via mountain uplift (Bryson Jr et al, 2012 ; Bryson Jr & Riddle, 2012 ; Castoe et al, 2009 ) or Pleistocene glacial cycles (Gutiérrez‐Rodríguez et al, 2022 )—dispersal into and out of Mesoamerica has also been a key factor structuring communities (López‐García & Morrone, 2022 ; Ornelas et al, 2014 ).…”