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Gene Flow and Environmental Differentiation Between Viviparous and Ovoviviparous Populations of Salamandra Algira Tingitana

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Gene Flow and Environmental Differentiation Between Viviparous and Ovoviviparous Populations of Salamandra Algira Tingitana Gene flow and environm ental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana Marco André Ferreira Dinis Mestrado em Biodiversidade, Genética e Evolução Departamento de Biologia 2016 Orientador Guillermo Velo-Antón, Investigador, CIBIO Coorientador Fernando Martínez-Freiría, Post-Doc, CIBIO Todas as correções determinadas pelo júri, e só essas, foram efetuadas. O Presidente do Júri, Porto, ______/______/_________ FCUP v Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana Agradecimentos Aos meus orientadores por esta oportunidade fantástica, pela disponibilidade e apoio demonstrados em todos os momentos, e pelo seu contagiante exemplo daquilo que um investigador deve almejar ser. Ao grande João Campos, o navegador exímio que descobriu a rota que me trouxe aqui, e que foi em diferentes momentos o meu batedor, mentor, anfitrião, consiglieri e amigo. Esta tese não existiria sem ti. Grazie mille, capo! Ao Doutor José Carlos Brito e a todos os elementos do Biodeserts pelo excelente acolhimento e pelo constante encorajamento à expansão de horizontes científicos. Ao André Lourenço, um agradecimento especial pelo inestimável apoio durante o trabalho de laboratório. E por não me deixar esquecer o Alentejo que me repousa na alma. Aos meus estimados companheiros de Mestrado, pelos quilómetros de estrada que palmilhámos juntos. Que venham muitos mais. À minha famíla, que mesmo à distância foi e será sempre o meu lar, epicentro e porto seguro. Este trabalho foi parcialmente financiado pelo projecto EVOVIV – Evolution of viviparity: an integrative framework for the study of an evolutionary novelty in Salamandra salamandra” (PTDC/BIA-EVF/3036/2012). FCUP vi Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana Index Agradecimentos v Index vi Table Index x Figure Index xii List of Abreviations xv Abstract xvii Resumo xix Chapter 1: General introduction 21 1.1 North Africa: an important biogeographic component of the Mediterranean Basin hotspot 22 1.2 The Salamandra genus 23 1.2.1 The North African Fire Salamander (Salamandra algira Bedriaga 1883) 24 1.2.2 Pueriparity in the Salamandra genus 26 1.2.3 Habitat and ecology of Salamandra algira 27 1.2.4 S. algira diversity in the Rif 29 1.3 Thesis structure and objectives: 30 1.3.1 Spatial patterns of genetic diversity in Rifean populations of S. algira (Manuscript I) 30 1.3.2 Historical and contemporary ecological niche of S. algira (Manuscript II) 31 1.3.3 Impact of landscape-change on habitat availability in a Palearctic relict in northern Maghreb (Manuscript III) 31 Chapter 2: Spatial patterns of genetic diversity in Rifean populations of S. algira (Manuscript I) 33 2.1 Introduction 34 2.2 Methods 35 FCUP vii Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana 2.2.1 Study area and sampling strategy 35 2.2.2 DNA extraction and amplification 36 2.2.3 Molecular analyses 38 2.3 Results 40 2.3.1 Field work and laboratory analyses 40 2.3.2 Phylogenetic analyses 41 2.3.3 Genetic structure and contact zones 44 2.4 Discussion 48 2.4.1 Phylogenetic relationships within Salamandra algira 48 2.4.2 Patterns of genetic diversity in the Rif 49 2.4.3 Evolutionary context of pueriparity 51 Aknowledgments 52 Chapter 3: Historical and contemporary ecological niche of S. algira (Manuscript II) 53 3.1 Introduction 54 3.2 Methods 56 3.2.1 Reconstruction of the biogeographic history of S. algira in North Africa and in the Rif 56 3.2.1.1 Data selection and preparation 56 3.2.1.2 Study area and variable selection 57 3.2.1.3 Ecological niche modeling 59 3.2.2 Present distribution of Rif lineages and relative importance of their niche components 60 3.2.2.1 Data selection and preparation 60 3.2.2.2 Development of combined models and identification of areas of sympatry 63 3.2.3 Ecological niche divergence and its role on the evolutionary differentiation among subspecies and within the Rif 64 FCUP viii Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana 3.3 Results 65 3.3.1 Reconstruction of the biogeographic history 65 3.3.1.1 ENMs for subspecies 68 3.3.1.2 ENMs for Rif sublineages 70 3.3.2 Present distribution and relative importance of niche components 71 3.3.2.1 Habitat models 71 3.3.2.2 Combined models and areas of sympatry 73 3.3.3 Niche divergence 75 3.4 Discussion 78 3.4.1 General biogeographic patterns 78 3.4.2 Biogeographic patterns of the Rif 79 3.4.3 Common ecological patterns 81 3.4.4 Current distribution of S. algira 83 3.4.5 Ecological implications for the evolution of pueriparity in S. algira 85 Chapter 4: Impact of landscape-change on habitat availability in a Palearctic relict in northern Maghreb (Manuscript III) 87 4.1 Introduction 88 4.2 Methods 90 4.2.1 Characterization of recent temporal trends in the variation of vegetation cover 90 4.2.2 Identification of natural areas most affected by vegetation loss 92 4.2.3 Identification of at-risk populations of S. algira 92 4.3 Results 93 4.3.1 Temporal patterns of vegetation change in North Africa 93 4.3.2 Vegetation loss by land cover class 98 4.3.3 At-risk populations of S. algira 99 4.4 Discussion 103 FCUP ix Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana 4.4.1 Global patterns of vegetation change 103 4.4.2 Landscape change and habitat degradation 104 4.4.3 Impact of vegetation loss on S. algira 107 4.4.4 Applicability to other Palearctic taxa 109 Chapter 5: Final remarks 111 Chapter 6: References 114 Chapter 7: Supplementary materials 135 FCUP x Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana Table Index Table 2.1 Genetic distances between mitochondrial lineages of S. algira. Highly differentiated values (>0.05) are outlined in bold. Sample size used for genetic distance estimation and haplotype network (N) and number of haplotypes per lineage (Hap) are also presented. SAT1: S. a. tingitana 1; SAT2: S. a. tingitana 2; SAT3: S. a. tingitana 3; SAS1: S. a. splendens 1; SAS2: S. a. splendens 2; SASA: S.a. spelaea; SAA: S. a. algira 44 Table 2.2 Pairwise FST values between clusters as assigned by STRUCTURE (Top half) and between mitochondrial lineages (bottom left). FST values are displayed below the diagonal, and probability based on 999 permutations above the diagonal. Descriptive statistics comparing the values by cluster and by lineage are also displayed (bottom right). K1-7: Cluster 1-7; tin1-3: S. a. tingitana lineages 1-3; spl1: S. a. splendens lineage 1; Avg: average; SD: Standard deviation; Max: maximum; Min: minimum 48 Table 3.1 Description, code, units and range (minimum and maximum) of the climatic and habitat variables used for model creation. Combined variables were the ones which contributed the most for climatic and habitat models and were thus used for the creation of combined models 64 Table 3.2 Number of occurrence records, average (and SD) training/test AUC and variable percentage contribution for the climatic models of the three S. algira subspecies and four Rif sublineages. SAA: S. a. algira; SAS: S. a. splendens; SAT: S. a. tingitana; SAT1: S. a. tingitana 1; SAT2: S. a. tingitana 2; SAT3: S. a. tingitana 3; SAS1: S. a. splendens 1 66 Table 3.3 Number of occurrence records, average (and SD) training/test AUC and variable percentage contribution for the habitat (top) and combined (bottom) models of the Rif sublineages. SAT1: S. a. tingitana 1; SAT2: S. a. tingitana 2; SAT3: S. a. tingitana 3; SAS1: S. a. splendens 1 74 Table 3.4 Results of niche identity and background tests for all S. algira subspecies and for the Rif sublineages, using the climate-only, habitat-only and combined (climate + habitat) models. Significant results (<0.05) are outlined in bold. D: Schoener’s D (Schoener, 1968); 1: background tests for which the empirical measurement of D is situated to the left of the null distribution. Alg: S. a. algira; spl: S. a. splendens; tin: S. a. tingitana; tin1: S. a. tingitana 1; tin2: S. a. tingitana 2; tin3: S. a. tingitana 3; spl1: S. a. splendens 1 77 Table 4.1 Percentage of the study area corresponding to distinct classes of relative net vegetation loss severity. Cumulative percentage is also displayed. 96 Table 4.2 Vegetation loss by type of land cover. All values are percentages. Total: percentage of study area occupied by land cover type; Loss LC: percentage of land cover type where vegetation loss was detected; Loss Total: percentage of the total vegetation loss corresponding to vegetation loss in the land cover type; S. algira occurrence records: percentage of S. algira occurrence records per land cover type. The last three lines summarize information for natural land cover excluding sparse vegetation areas, all natural land cover and non-natural (i.e. agricultural) land cover 101 Table 7.1 Characteristics of the 13 microsatellites used in this study. Information regarding multiplex arrangement, original published primer forward and reverse sequences, fluorescently labelled FCUP xi Gene flow and environmental differentiation between viviparous and ovoviviparous populations of Salamandra algira tingitana oligonucleotides used as template for modified forward primers and the concentration of primer forward and reverse used to construct multiplex mixes and on 10 µl PCR reactions are represented. (Adapted from Álvarez et al., 2015) 136 Table 7.2 Identification and location of all samples collected and cytochrome b (cyt-b) and β- fibrinogen (β-fibint7) sequence data used in this work.
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