André Vincente Liz: PhD defense

André Vincente Liz: PhD defense

Comparative phylogeograpy of the Sahara – Sahel: a spatiotemporal approach to biodiversity dynamics in the largest warm desert on erth

Our PhD Student André Vincente Liz just successfully defended his PhD thesis, congratulations! A full recording of the defense is provided by the University of Porto.

Abstract

The Sahara-Sahel environments are home to rather endemic desert biotas highly adapted to the region’s aridity constraints and the dry/humid climatic cycles that took place throughout the Plio-Pleistocene. Species’ contemporary patterns harbour a crucial potential to understand the impacts of these steep fluctuations on the desert’s landscape, as well as to develop integrative conservation agendas that help preserving a highly vulnerable local wildlife. Yet, this baseline biological knowledge has been traditionally lacking for the region. With the advent of molecular phylogeography at the end of the 20th century, biodiversity studies in the Sahara-Sahel have started unravelling novel aspects of its intricate natural history, primarily how palaeoclimatic and subsequent land-cover shifts have shaped the distribution and genetic structure and diversity of local species by triggering different eco-evolutionary processes. Core biogeographic and evolutionary hypotheses have been posed, including population divergence in allopatry, which often led to speciation, dispersal and colonisation of new environments, including trans-Saharan migrations across the desert, or events of secondary contact. Notwithstanding the remarkable recent advances in regional research, biodiversity patterns in some of the most unique features within the region’s eco-physiographic diversity remain virtually unknown. Besides, the phylogeographic scenarios that have been proposed lack corroboration under a common framework.

Aiming to provide the first comprehensive picture of biodiversity patterns in the Sahara-Sahel, this thesis builds upon a comparative phylogeography framework that seeks to verify and expand the major biogeographic and evolutionary questions posed for the region. For this purpose, I assessed all publicly available DNA data for Sahara-Sahel vertebrates (i.e., >1,000 species) and selected the most relevant taxa based on data availability and species’ distribution within the study area. I tested phylogeographic scenarios through the integration of different molecular and eco-geographic analyses, including phylogenetics, phylogeography, population genetics, species distribution modelling (SDM), and geostatistics. These analyses allowed inferring the location of ecological refugia, dispersal corridors, and hotspots of intra-specific diversity for regional species according to their habitat requirements, i.e. those more- (xeric) or less (mesic) adapted taxa to the desert’s extreme aridity. Considering that the advent of arid conditions in North Africa triggered the diversification of the most xeric taxa, examining the phylogenetic ages of these species allowed estimating the chronology of the Sahara for the first time from a biological point of view. During the development of this thesis, I also generated new biodiversity data that allowed examining phylogeographic hypotheses in poorly known regions of the Sahara-Sahel, which yet constitute key elements to understand the region’s natural history. Specifically, I (1) addressed the role of Central Sahara highlands in historical biodiversity dynamics, and (2) examined biodiversity patterns throughout the hyper-arid Sahara.

Notably, the phylogenetic insights brought by xeric taxa suggest that the onset of aridification in North Africa occurred in the Mid Miocene, contrasting remarkably with geological and climatological findings. The age of the Sahara is still a controversial topic; evidence for this is that new studies keep reporting contrasting estimates: from 7 up to 11 Myr. This thesis provides the first comprehensive chronology for the impact of regional aridification on Saharan wildlife. Beyond vertebrates, this work also looked at the age of the remaining taxonomic groups for which molecular data was available (i.e., scorpions), given the low number of species that occupy the desert’s extreme environments. This analysis highlighted the need for systematic assessments on Saharan xeric arthropods, such as beetles, spiders or grasshoppers, which present profound knowledge shortfalls despite being major elements within the region’s biological diversity.

Concerning the lack of phylogeographic knowledge for some of the least known regions of the Sahara-Sahel, two studies were conducted. In the first one, I assessed whether the mountains of Central Sahara acted as historical ecological refugia and diversification hotspots for mesic taxa, while also aided in trans-Saharan faunal translocations during humid desert stages. Insights come from the phylogeographic assessment of Acanthodactylus boskianus, a species complex inhabiting mesic environments and distributed at both sides of the desert and in scattered populations throughout the Central Sahara highlands. Results revealed that mountains in Southern Algeria (i.e., Tassili N’Ajjer, Ahaggar), South-western Libya (i.e., Fezzan, Akakus), Niger (i.e., Aïr), and Northern Chad (i.e. Tibesti) harbour historical climatic stability that favoured the local persistence of A. boskianus. Besides, the few genetic samples available from the region recovered high local lineage diversity, with reports of old and mountain endemic clades. Lack of genetic differentiation between some Mediterranean, Central Saharan, and Sahelian populations suggest the existence of recent gene flow between both sides of the desert, which could be explained through the intermittent ecological suitability here observed across interconnected Central Sahara mountainous refugia. In the second study, I analysed the genetic structure and diversity of species inhabiting the most arid environments of the Sahara, where knowledge on biodiversity patterns was almost inexistent. For this purpose, I conducted a phylogeographic assessment of the Acanthodactylus scutellatus complex, which embeds six currently recognised species that possibly comprise the most widespread vertebrates across hyper-arid Saharan habitats. Results recovered surprisingly high levels of intra-specific diversity, including several previously unknown sympatric or parapatric lineages that exhibit both nuclear and mitochondrial differentiation, suggesting species status. These findings evidence that biodiversity estimates for xeric Saharan habitats are likely neglecting a notable amount of undescribed diversity, which seemingly originated in allopatry due to the steep habitat fluctuations that took place throughout the Plio-Pleistocene. Interestingly, the origin of some of these lineages dates back to the Miocene, coinciding with the onset of dry/humid fluctuations in North Africa. Some environments of the northern Sahara, such as the Algerian ergs (i.e., sand-dune fields), were found to be particularly rich in terms of intra-specific diversity. A contrasting pattern was found across southern Sahara latitudes and the Sahel, where the lack of genetic differentiation between distant populations suggested that population dispersal at this latitude was common. The assessment of individual lineage genetic imprints allowed delimiting potential areas of refugia within these desert corridors, however, fine-scale research is needed to clarify whether they correspond to specific landscape features such as palaeolakes, ergs or mountain outskirts.

The primary component of this thesis was the comparative phylogeography assessment, which I conducted after setting the biological chronology of the desert, generating additional data, and refining key phylogeographic hypotheses. This meta-analysis was conducted through the integration of molecular and ecological components for 107 selected desert taxa, including reptiles, mammals, amphibians, and scorpions. During this process, roughly 8,500 DNA sequences were analysed, most of them corresponding to published data retrieved from GenBank and some newly produced to fill key taxonomic and geographic gaps. The analyses of DNA information allowed estimating areas of high genetic diversity and connectivity for each individual species, as well as for the mesic and xeric communities. The molecular component was integrated with an SDM approach, which expanded the methodological framework traditionally applied to biodiversity assessments in the deserts of North Africa. As such, I incorporated for the first time historical hydrological and vegetation data into the SDM pipeline, thus considering previously overlooked ecological dimensions which likely played a major role in historical species responses to dry/wet fluctuations. The historical shifts in species’ range were modelled for the selected 107 taxa using over 28,000 observation records. Results allowed verifying the major biogeographic and evolutionary questions previously proposed for the region. Patterns of intra-specific diversity confirm that the isolated mountains of Central Sahara are important centres of diversity, several of which still lack baseline biodiversity knowledge, with clear examples in Chad (i.e., Tibesti, Ennedi) and Sudan (i.e., Jabal Marrah). High diversity was also found across the northern Sahara for xeric taxa, suggesting that this region harbours a crucial role in the evolution and persistence of truly-desert species, despite local biodiversity patterns being also poorly known. Refugia inferences corroborate the importance of the Atlantic region for most of the species, as well as northern Sahara areas for xeric taxa and mountains for mesic taxa. Additionally, patterns of genetic and ecological connectivity confirm that corridors across Central Sahara highlands played a major role in trans-Saharan dispersals, which can be comparable to that of the Nile Valley and the Atlantic Coast.

This thesis provides integrative knowledge that can be immediately applied to biodiversity conservation agendas in the deserts of North Africa, as well as to the study of biodiversity in deserts and arid regions. In addition, insights on species’ genome and habitat imprints expand our understanding of the natural history of the region, with implications for the evolution and migration of both the desert’s endemic biotas and the early humans that peopled the Sahara and dispersed out of Africa at the end of the Quaternary. Besides, this thesis opened new biogeographic and evolutionary questions that would require additional research efforts, as well as pinpointed areas of dramatic biodiversity shortfalls that should be targeted in future studies.

Parts of his thesis are already published:

Liz, A. V., D. Rödder, D. V. Gonçalves, G. Velo-Antón, M. M. Fonseca, P. Geniez, P.-A. Crochet, and J. C. Brito. 2023. Overlooked species diversity in the hyper-arid Sahara Desert unveiled by dryland-adapted lizards. Journal of Biogeography 50: 101–115. (PDF)

Liz, A. V., D. V. Gonçalves, G. Velo-Antón, J. C. Brito, P.-A. Crochet and Rödder, D. 2022. Adapt biodiversity targets to climate change. Science 376: 589-590. (PDF)

Liz, A. V., D. Rödder, D. V. Gonçalves, G. Velo-Antón, M. M. Fonseca, P. Geniez, P.-A. Crochet, and J. C. Brito. 2021. The role of Sahara highlands in the diversification and desert colonisation of the Bosc’s fringe-toed lizard. Journal of Biogeography 48: 2891–2906.

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