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Dynamic historical climatic variation as a driver of diversification in chameleons endemic to the Congo basin and the montane rainforests of central African “sky-islands”
Tapondjou Nkonmeneck, Walter Paulin
Tapondjou Nkonmeneck, Walter Paulin
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Abstract
With one of the highest biodiversity hotspots on earth, the African rainforest is one of the most important in the world. Going from luxurious rainforests to majestic mountains, it is home to nearly one-fifth of the world's diversity. One of the primary goals of the evolutionary biologist is to elucidate how and when African rainforest diversity arose and understand how biodiversity is generated and maintained. In West-Central Africa, the Guineo-Congolian rainforest makes up most of the tropical rainforest, and the highest diversity is found along the Cameroon Volcanic Line (CVL). The CVL represents biological 'sky islands' providing the ideal opportunity to understand how orogenesis and historical climate change influenced species diversity and distribution in these isolated African highlands. These mountains have been the focus of substantial effort from researchers to understand the evolution of its distinctive biota. A combination of diverse analytical resources such as phylogeography, population genomics, and paleoecology can be used to understand how genes, geography, and ecology interact to generate, maintain, and distribute biodiversity.A few montane endemic species (primarily birds, mammals, and trees) from West-Central Africa have been studied to characterize and identify the evolutionary processes responsible for nowadays diversity in the CVL. However, very few of them used reptiles as a study system. Chameleons are one of the rare reptile species endemics of the montane forest of the CVL. Their low vagility, high morphological diversity, and extreme sensitivity to microclimate changes make them a fascinating study system. Chapter 1 aims to characterize the geographical basis of genetic variation in an anomalously distributed species Rhampholeon spectrum. This chapter uses multi-locus Sanger data and genomic sequences to explore population structure and range-wide phylogeographic patterns in R. spectrum. We then employ demographic analyses and niche modeling to distinguish between alternate explanations, hypothesized to potentially contextualize the impact of past geological and climatic events on the present-day distribution of intraspecific genetic variation in this endemic West-Central African vertebrate lineage. Allopatric speciation, congruent with isolation caused by geologic uplift of the East African rift system (the “descent into the Icehouse” and aridification of sub-Saharan Africa during the Eocene-Oligocene), is identified as the fundamental model to explain the population divergence between R. spectrum and its closely related sister clade from the Eastern Arc Mountains. Throughout the range of R. spectrum, our finding of pronounced geographically based population structure suggests that divergence and, potentially, isolation and speciation began between the late Miocene and the Pleistocene. Phylogenetic analyses suggest that R. spectrum is a complex of five geographically delimited populations grouped into two major clades (montane vs. lowland). Sea level changes during the Pleistocene climatic oscillations resulted in allopatric speciation associated with dispersal over an ocean channel barrier and colonization of Bioko Island. Demographic inferences and range stability mapping support diversification models with secondary contact due to population contraction in lowland and montane refugia during the interglacial period. Our results unveil R. spectrum’s genetic diversity north of the Sanaga River and within the Island of Bioko and highlight the urgent need to ameliorate one of the most substantial obstacles to our understanding of the diversity, distributions, and conservation status of Central African vertebrates: the lack of genetic material from the Congo Forest. Chapter 2 investigates the evolutionary history and historical biogeography of the West-Central Africa Trioceros. Molecular studies of inter-and intra-specific diversity and species relationships, when integrated with more traditional approaches of biogeography and paleoecology, have much to contribute to this understanding of the evolutionary processes that generate and sustain diversity in tropical faunas. Here we study the phylogenomic clade of the mountain endemic African horned chameleons. We use a combination of mitochondrial DNA (mtDNA) and genome-wide restriction site-associated DNA sequencing (RADseq; nDNA hereafter). We inferred a time-calibrated mtDNA gene tree, nDNA species trees, and phylogenetic networks. Our data reveal three introgression events that explain the mito-nuclear discordance obtained with our phylogenetic inferences. Historical and recent climatic oscillations which can fragment, expand, and contract species distributions followed by rapid radiation are discussed here as the most plausible explanation for this phenomenon. Chapter 3 identifies the ecomorphological traits observed in the genus Trioceros, hoping to reveal the patterns and drivers responsible for diversification in living organisms. However, different ecomorphological traits can evolve at different paces and respond differentially to selective pressures. This study uses a multispecies coalescent method to generate the first most complete phylogenetic tree for the African horned chameleon genus Trioceros. We explore the patterns of evolutionary change for the following ecomorphological traits: Cranial protuberance, gular and dorsal crest, horn count, Boy size and tail ratio, habitat use, and altitudinal distribution. We use different phylogenetic comparative methods to search for evolutionary relationships between traits and estimated ancestral states, rates of evolution, and the amount of phylogenetic signal on each trait. Our results suggest that None of the traits follow the irreversibility law (Dollo’s law) as they are all gained and lost through time. The evolution of cranial protuberance (horn presence or absence, type and number of horns) is independent from phylogenetic relationships. Other morphological features such as the gular and dorsal crest, which have evolved multiple times and transitioned from one state to another, seem to be associated with the inferred phylogeny. We detect an association between morphological and ecological traits, with Trioceros following the Rensch’s rule with more prominent individuals tend to have more ornament. More prominent species associated with a high count of morphological ornaments play an important role in species signaling, male combat, and reproductive purposes. Chapter 4 looks at the current knowledge of sex chromosome evolution in chameleons, emphasizing species from two genera, Rhampholeon and Trioceros, from continental Africa with an unknown chromosome system. This study attempts to identify the sex chromosome systems of Rhampholeon spectrum, Trioceros montium, and T. quadricornis subsp. We use sex-specific RAD markers obtained from RAD sequences, a proven method that has emerged recently as an efficient tool to investigate sex chromosomes. Moreover, the recently developed program RADSex identifies and extracts sex-linked RAD loci that are subsequently validated using PCR. We demonstrated here that the program RADSex is an impressive tool for deciphering sex chromosome systems from RADseq data by its ability to generate nonpolymorphic markers. We successfully identified ZZ/ZW sex markers in Trioceros montium and Rhampholeon spectrum, suggesting independent evolution of sex chromosome systems within these genera. We then discuss these results and suggest the ZW system could be more common in the genus Trioceros pending further investigation of other species.
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Date
2022-08-31
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University of Kansas
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Keywords
Biology, Systematic biology, Cameroon Volcanic Line, Chameleon, Phylogeography, Rhampholeon, Sex chromosomes, Trioceros