Genomic analyses of speciation and hybridization in giraffe

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The genus Giraffa likely originated around seven million years ago in Indo-Asia, migrating into Eastern Africa via the Arabian-African land bridge. This migration coincided with a major environmental transition from forested landscapes to savannah and shrubland ecosystems. This ecological shift likely drove the evolution of Giraffa’s distinctive adaptations, such as elongated necks and legs, which enabled high browsing and improved predator vigilance. Over millions of years, at least five giraffe species emerged in Africa, though only Giraffa camelopardalis persisted into modern times. Fossil evidence places this species in East Africa about 1 Mya, from where it expanded to its current range across the continent. Despite their ecological significance and widespread recognition, giraffe biology and genetics have been relatively underexplored compared to other large mammals. For much of the 20th century, modern giraffe were classified as a single species (G. camelopardalis) divided into multiple subspecies based on morphology and geographic distribution. However, recent genetic studies based on microsatellites and a few mitochondrial and nuclear sequences have challenged this view, proposing the existence of up to four distinct giraffe species: G. camelopardalis, G. reticulata, G. tippelskirchi, and G. giraffa. A relatively recent divergence and partially overlapping ranges further blur the limits between giraffe (sub)species by bringing into question the weight of gene flow and hybridization in their evolution. While these processes were classically seen as obstacles to species divergence, it is now recognized that they play an important role in the evolutionary continuum, which complicates traditional approaches to species delimitation. These findings highlight the gaps in knowledge about this species and may have significant implications for taxonomy, evolutionary biology, and conservation. Meanwhile, giraffe populations face escalating threats such as habitat loss, poaching, and environmental changes. On the other hand, conservation strategies are hindered by an unclear taxonomy. A clear taxonomy would allow prioritizing resources and securing a healthy gene pool by preserving genetically distinct populations. Thus, to resolve this taxonomic uncertainty and inform the conservation efforts, a robust, comprehensive approach is called for. This doctoral dissertation aims to investigate speciation, hybridization, and genetic diversity through state-of-the-art genomic approaches and address key questions on giraffe taxonomy and evolution, which may, in turn, provide valuable insights for preserving this iconic species. REALIZED STUDIES In Publication 1 (Coimbra et al. (2021), Current Biology 31, 2929–2938), I de novo assembled the genome of the critically endangered Kordofan giraffe (Giraffa camelopardalis antiquorum) using 10X Genomics’ linked-reads technology, and investigated the population structure and speciation in giraffe (Giraffa spp.) using whole-genome sequencing data from 50 individuals representing all currently recognized giraffe subspecies. The population genomic and phylogenomic analyses implemented in the study support the existence of four separately evolving giraffe lineages with distinct demographic histories, which correspond to the four species proposed by Fennessy et al. (2016). No significant signals of hybridization were found between those lineages in wild individuals, but three captive reticulated giraffe (G. reticulata) showed signs of either admixture or mitochondrial introgression. The four lineages revealed here conform to the broader Unified Concept of Species and are consistent with long-term reproductive isolation (albeit incomplete), the primary criterion for delineating species under the Biological Species Concept. These findings provide a solid genomic basis for the recognition of four distinct species of giraffe and highlight the need for a revision of the giraffe taxonomy adopted by the International Union for Conservation of Nature (IUCN), and consequently, a re-evaluation of their conservation status, which would likely result in higher threat categories for three of the four species. In Publication 2 (Coimbra et al. (2023), BMC Biology 21, 215), I assessed the occurrence and the extent of natural hybridization and genetic admixture among the three giraffe taxa ranging in East Africa—namely Nubian (G. c. camelopardalis), reticulated (G. reticulata), and Masai giraffe (G. tippelskirchi tippelskirchi). I analyzed complete nuclear and mitochondrial genomes of 128 wild giraffe sampled mostly across Kenya, where these taxa are parapatric and contact zones have been anecdotally reported (i.e., Laikipia Plateau, and the area south of Garissa towards the Tsavo region). The reticulated giraffe showed varying levels of Nubian ancestry in 13 individuals sampled across the Laikipia Plateau most likely reflecting historical gene flow between these two lineages. Although comparatively weaker signs of ancestral gene flow and potential mitochondrial introgression from reticulated into Masai giraffe were also detected, estimated admixture levels between these two lineages are minimal. Importantly, contemporary gene flow between East African giraffe lineages was not statistically significant. Effective population sizes have declined since the Late Pleistocene, more severely for Nubian and reticulated giraffe. Despite historically hybridizing, these three giraffe lineages have maintained their overall genomic integrity suggesting effective reproductive isolation and supporting their classification as separate species.

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