Isolation by distance and past climate resistance shaped the distribution of genealogical lineages of a neotropical lizard

Abstract

Organisms adapted to open environments in South America have recently been used to understand the origins of the high Neotropical biodiversity. In the Caatinga, the largest continuous block of Seasonally Dry Tropical Forest in South America, phylogeographic studies have uncovered the role of historical climate changes and rivers (i.e., the São Francisco River, the largest perennial river in Caatinga), in promoting genetic differentiation and speciation of lizards and amphibians. We used mitochondrial data, demographic analyses, paleodistribution models, and landscape genetic methods to test the effects of spatial distances, historical climate fluctuations, and landscape heterogeneity on the genetic variation of the generalist lizard Tropidurus hispidus in the semi-arid Caatinga in northeastern Brazil. Four haplogroups with moderate geographical structure diverged in the Pleistocene, and exhibited high genetic diversity. Ecological niche models revealed large suitable climatic areas for T. hispidus in the past 790 thousand years, connecting the Caatinga and other regions via a narrow corridor. Part of the genetic differentiation in T. hispidus resulted from spatial distances among populations and isolation by resistance through climatic unsuitability areas in the Last Glacial Maximum (LGM), which probably reduced population connectivity and gene flow. Our findings highlight the role of the historical factors of the Caatinga, through LGM climate, and the generalist condition of species in shaping the genealogical histories of populations. Although the results are based on a single-locus approach, our study is a first step to shed light on the main drivers of the evolutionary history of T. hispidus, in a highly diverse and still poorly studied region.

Key words:

• Caatinga
• Espinhaço Mountain Range
• isolation by resistance
• landscape genetics
• Seasonally Dry Tropical Forests
• Tropiduridae
• Tropidurus hispidus

Acknowledgments

FC thanks FUNDECT (Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for financial support and his post doc fellowship (processes # 71/700.083/2020; 302162/2020-8). AAG thanks CNPq (processes 552031/2011-9, 431433/2016-0, and 310942/2018-7) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; processes 23038.005577/2012-28 and 23038.009565/2013-53) for financial support. DOM thanks CNPq for a research fellowship (process 306541/2017-3). GRC thanks CAPES, CNPq, FAPDF (Fundação de Apoio à Pesquisa do Distrito Federal), and the USAID’s PEER program under cooperative agreement AID-OAA-A-11-00012 for financial support. We thank Instituto Chico Mendes de Conservacão da Biodiversidade (ICMBio) for collecting permits.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental material

Supplemental material for this article may be accessed here: https://doi.org/10.1080/14772000.2022.2084470.

Data availability statement

All sequences will be deposited in GenBank (accession numbers: to be added).

Associate Editor: Dr Susan Tsang

Additional information

Funding

This work was funded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico; processes 302162/2020-8, 552031/2011-9, 431433/2016-0, and 310942/2018-7), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; processes 23038.005577/2012-28 and 23038.009565/2013-53), FUNDECT (Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul; process # 71/700.083/2020), and FAPDF (Fundação de Apoio à Pesquisa do Distrito Federal) and the USAID’s PEER program under cooperative agreement (Award Number AID-OAA-A-11-00012).