Allopatric diversification and evolutionary melting pot in a North African Palearctic relict: The biogeographic history of Salamandra algira

Arlo Hinckley,James D Burgon,Kathryn R Elmer,Sebastian Steinfartz,David Donaire,Marco Dinis,Tahar Slimani,Adnane Fawzi,Ulrich Joger,Guillermo Velo-Antón,Khaled Merabet,Fernando Martínez-Freiría,Soumia Fahd,Miguel Vences

doi:10.1016/j.ympev.2018.10.018

Abstract

North Africa is a climatically and topographically complex region with unique biotic assemblages resulting from the combination of multiple biogeographic realms. Here, we assess the role of climate in promoting intra-specific diversification in a Palearctic relict, the North African fire salamander, Salamandra algira, using a combination of phylogenetic and population genetic analyses, paleoclimatic modelling and niche overlap tests. We used mitochondrial DNA (Cyt-b), 9838 ddRADseq loci, and 14 microsatellite loci to characterize patterns of genetic diversity and population structure. Phylogenetic analyses recover two major clades, each including several lineages with mito-nuclear discordances suggesting introgressive patterns between lineages in the Middle Atlas, associated with a melting pot of genetic diversity. Paleoclimatic modelling identified putative climatic refugia, largely matching areas of high genetic diversity, and supports the role of aridity in promoting allopatric diversification associated with ecological niche conservatism. Overall, our results highlight the role of climatic microrefugia as drivers of populations’ persistence and diversification in the face of climatic oscillations in North Africa, and stress the importance of accounting for different genomic regions when reconstructing biogeographic processes from molecular markers.

Highlights

North Africa is a climatically and topographically complex region, characterized by Mediterranean climate in the north and arid Saharan climate in the south
The cytochrome b gene (Cyt-b) tree identified two major clades: a western clade comprising two monophyletic groups corresponding to the subspecies S. a. tingitana (NW Moroccan Rif) and S. a. splendens (SW and Central Rif and Middle Atlas), and an eastern clade comprising S. a. spelaea in the Moroccan Beni Snassen massif and S. a. algira in Algeria; Figs. 2 and S3.2)
Delimitation of subspecies within the eastern clade was hindered by the paraphyletic status of S. a. algira, due to a sister-group relationship between the westernmost Algerian population from Chrea and S. a. spelaea from Beni Snassen (Fig. S3.2), possibly caused by insufficient phylogenetic information in this short mitochondrial DNA (mtDNA) segment

Summary

Introduction

North Africa is a climatically and topographically complex region, characterized by Mediterranean climate in the north and arid Saharan climate in the south. Its location at the intersection of distinct biogeographic regions produces a unique species composition (Dobson and Wright, 2000). For Mediterranean lineages in particular, aridity has been a main driver of population fragmentation and subsequent divergence (Cosson et al, 2005), especially from the mid-Pliocene to the Pleistocene when the region regularly experienced alternating humid and hyper-arid phases (Quezel and Barbero, 1993). Two predominant biogeographic patterns can be observed for Mediterranean species in North Africa. Veith et al, 2004) or with periods of climatic fluctuations ranging from humid to hyper-arid conditions The second, is a tendency for intraspecific divergence along a west-east axis (e.g. Beukema et al, 2010; Velo-Antón et al, 2012; Stuckas et al, 2014; Beddek et al, 2018), likely associated with historical marine transgressions into river valleys (e.g. Veith et al, 2004) or with periods of climatic fluctuations ranging from humid to hyper-arid conditions

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