Phylogenomics, Species Discovery and Integrative Taxonomy in Dalbergia (Fabaceae) Precious Woods from Madagascar

Abstract

Understanding the evolution of biological diversity is of fundamental interest to molecular ecologists and conservation biologists. In particular in biodiversity hotspots, major knowledge gaps exist regarding the numbers of species, their morphological distinction, ecology, distribution and risk of extinction, as well as their possible commercial value and use. The pantropical genus Dalbergia L.f. (Fabaceae) includes precious timber species known as rosewoods or palisanders, many of which are threatened by habitat degradation and often illegal selective logging. The use of existing species circumscriptions and application of available identification keys is particularly challenging in Madagascar, where a large number of closely related species co-occur and where the reliance on flower and fruit characters for identification is high, even though these structures are often absent on living specimens. The resulting taxonomic uncertainties have important implications for national and international trade regulations and impede the setting of conservation priorities. The aim of this Ph.D. thesis was to increase our understanding of the number, morphological distinction and phylogenetic relationships between the Dalbergia species present in Madagascar. Towards this goal, I developed a genome-wide DNA analysis approach that I used in combination with morphological and eco-geographic analyses. In the first chapter, my collaborators and I explored the utility of target enrichment sequencing to assess genetic variation in Dalbergia at the level of populations and closely related species, and between divergent species within the genus. Specifically, we assessed the sequence capture sensitivity and specificity of 7,201 candidate genomic regions with a conserved core across available genomes of Papilionoideae, and identified 2,396 regions that can be efficiently recovered for genomic analyses across Dalbergia. We also explored the performance of the 7,201 candidate regions across legumes, and identified 1,005 target regions that can be efficiently recovered for analyses at the family level. These confirmed high levels of gene tree discordance, previously reported also by other authors, especially near the root of the family. Furthermore, our analyses resulted in the development of a general-purpose bioinformatics pipeline for scalable, streamlined and reproducible analysis of such genome-wide and complex datasets. In the second chapter, we employed the developed genomic and bioinformatic resources for species discovery within the genus Dalbergia from Madagascar and the Comoros. This led to the confirmation of 46 out of 49 already described and accepted species as separately evolving lineages, while three currently accepted species were identified as potential synonyms. Furthermore, we discovered 49 new candidate species, of which 14 could be delimited as separately evolving from one another and from the confirmed described species. Lineage separation could not be conclusively assessed for the remaining 35 candidate species because of a currently insufficient availability of high-quality collections. Phylogenomic analysis confirmed the existence of two diverse clades of Malagasy Dalbergia, one of which appears to be associated with a clade of species from continental Africa, as well as an isolated lineage, which also occurs in continental East Africa. It further revealed a fourth lineage present in Madagascar, which is connected to another clade of species from continental Africa, and a biogeographic connection between species of West Madagascar and the Comoros. In the third chapter, we completed the integrative taxonomic workflow for three confirmed evolutionary species of high conservation concern. Specifically, we newly described D. pseudomaritima Crameri, Phillipson & N. Wilding and D. razakamalalae Crameri, Phillipson & N. Wilding as distinct species occurring in littoral and low-elevation evergreen humid forests in southeast Madagascar, and emended the description of D. maritima R. Vig. from central-east Madagascar to exclude the two south-eastern species, with which it had previously been confused. For all three species we also performed conservation assessments according to the IUCN Red List categories and criteria, and assigned the category Endangered (EN) to all of them. A major result from this dissertation is the finding that the diversity of Dalbergia species in Madagascar has hitherto been vastly underestimated. Thanks to major recent efforts to sample and document Dalbergia species, and the developed sequence capture and high-throughput DNA sequencing approach, which provides unprecedented phylogenomic resolution, part of the species diversity existing in Madagascar could be uncovered. In combination with morphological and eco-geographic data we were able to show that several threatened species are not currently represented in existing protected areas and that some highly exploited species with presumably large distribution ranges are actually composed of several species with much narrower distribution ranges. These findings call for further investigations and conservation action, and provide scientific evidence that will hopefully foster science-based conservation efforts.