Biogeographic and demographic history of the Mediterranean snakes Malpolon monspessulanus and Hemorrhois hippocrepis across the Strait of Gibraltar

Abstract

Background The contribution of North Africa to the assembly of biodiversity within the Western Palaearctic is still poorly documented. Since the Miocene, multiple biotic exchanges occurred across the Strait of Gibraltar, underlying the high biogeographic affinity between the western European and African sides of the Mediterranean basin. We investigated the biogeographic and demographic dynamics of two large Mediterranean-adapted snakes across the Strait and assess their relevance to the origin and diversity patterns of current European and North African populations. Results We inferred phylogeographic patterns and demographic history of M. monspessulanus and H. hippocrepis, based on range-wide multilocus data, combined with fossil data and species distribution modelling, under present and past bioclimatic envelopes. For both species we identified endemic lineages in the High Atlas Mountains (Morocco) and in eastern Iberia, suggesting their persistence in Europe during the Pleistocene. One lineage is shared between North Africa and southern Iberia and likely spread from the former to the latter during the sea-level low stand of the last glacial stage. During this period M. monspessulanus shows a sudden demographic expansion, associated with increased habitat suitability in North Africa. Lower habitat suitability is predicted for both species during interglacial stages, with suitable areas restricted to coastal and mountain ranges of Iberia and Morocco. Compiled fossil data for M. monspessulanus show a continuous fossil record in Iberia at least since the Pliocene and throughout the Pleistocene. Conclusions The previously proposed hypothesis of Pleistocene glacial extinction of both species in Europe is not supported based on genetic data, bioclimatic envelopes models, and the available fossil record. A model of range retraction to mountain refugia during arid periods and of glacial expansion (demographic and spatial) associated to an increase of Mediterranean habitats during glacial epochs emerges as a general pattern for mesic vertebrates in North Africa. Moreover, the phylogeographic pattern of H. hippocrepis conforms to a well-established biogeographic partition between western and eastern Maghreb.

Comparison and Synthesis of Sea‐Level and Deep‐Sea Temperature Variations Over the Past 40 Million Years

“…Sea level records, together with deep‐sea temperature records, are also essential for (b) improving insights into the processes involved in changing Earth's long‐term climate state (e.g., Boettner et al., 2021; DeConto & Pollard, 2003; De Vleeschouwer et al., 2017; Foster & Rohling, 2013; Katz et al., 2008; K. G. Miller et al., 2020; Rohling et al., 2021; Westerhold et al., 2020); and (c) assessing whether, and to what extent, Earth's climate sensitivity to radiative forcing changes depended on the initial climate state, with relevance for anthropogenic climate change (e.g., Hansen et al., 2007, 2008; Köhler et al., 2010; Masson‐Delmotte et al., 2010; PALAEOSENS, 2012; Rohling et al., 2012, 2018; Stap et al., 2018; von der Heydt et al., 2016). Finally, enhanced understanding of sea‐level change supports: (d) quantification of coastal stability related to vertical crustal movements, including the influences of mantle dynamic topography and glacio‐isostatic adjustments (for references, see Section 2); and (e) improved determination of the drivers of past biogeographic and paleo‐anthropological migration, isolation, and diversification patterns (e.g., Abbate & Sagri, 2012; Adeleye et al., 2021; Armitage et al., 2011; Bailey, 2010; Elias et al., 1996; Fernandes et al., 2006; Gibert et al., 2003; Hill et al., 2022; Hölzchen et al., 2022; G. E. Lee et al., 2020; Machado et al., 2021; Molina‐Venegas et al., 2015; Qi et al., 2014; Rohling, Grant, et al., 2013; Rolland, 2013).…”

First occurrence of Psammophis (Serpentes) from Europe witnesses another Messinian herpetofaunal dispersal from Africa – biogeographic implications and a discussion of the vertebral morphology of psammophiid snakes

“…Herpetofaunal exchanges between Mediterranean Africa and Europe during (or around) the Messinian Salinity Crisis have already been suggested for several reptile and amphibian groups (see extensive discussion in Georgalis et al, 2019). Especially in the Western Mediterranean area, herpetofaunal dispersal events between Maghreb and Iberia during the Messinian (but also earlier, during the Tortonian) had taken place, as it is also evidenced by molecular studies on various amphibian and reptile groups that currently inhabit both these areas (e.g., scincid and lacertid lizards, colubrids, and Malpolon : Carranza et al, 2004, 2006; Harris et al, 2004; Mendes et al, 2017; Machado et al, 2021).…”

Lack of country-wide systematic herpetology collections in Portugal jeopardizes future research and conservation

“…The absence of new accessioned specimens does not reflect the current landscape of studies regarding Portuguese herpetofauna. In the last fifteen years, several studies addressed the phylogeography and biogeography of Portuguese herpetofauna (Ambu et al 2023, Camacho-Sanchez et al 2020, Faria et al 2021, Machado et al 2021, Marques et al 2022b, Pinho et al 2009, Rato et al 2013, 2016, Sampaio et al 2014, Santos et al 2012a, b, Vences et al 2014, its morphology and physiology (Enriquez-Urzelai et al , Kaliontzopoulou et al 2012, Lucchini et al 2020, Marques et al 2022a, Martínez-Castro et al 2021, Martínez-Gil et al 2022, Massetti et al 2017, Pinho et al 2022, the revision of long-standing taxonomic and nomenclatural problems (Arntzen 2018, Arntzen et al 2021, Ceríaco & Bauer 2018, Caeiro-Dias et al 2018, Dubois & Raffaëlli 2009, Geniez et al 2014, Sequeira et al 2019, the impact of pathogens on natural populations (De Sousa et al 2012, Rosa et al 2022, Stöhr et al 2015, Thumsová et al 2022, and even the description of new species (Dias-Rodríguez et al 2017, Geniez et al 2014, Fitze et al 2012. However, the majority of specimens used in these studies were either not deposited in Portuguese NHCs or voucher specimens were simply not collected at all and instead substituted by non-lethal methods such as a tail and/or toe clipping and photographs.…”