International initiatives aimed at generating genomic resources, and particularly reference genomes, have flourished in recent years. Some focus on specific taxa, such as the Vertebrate Genomes Project, Bird Genome 10K Project, Bat1K Project, Global Invertebrate Genomics Alliance, 10 000 Plant Genomes Project, and 1000 Fungal Genomes project. Others focus on geographic regions, such as the California Conservation Genomics Project, Darwin Tree of Life for Britain and Ireland, Catalan Initiative for the Earth BioGenome Project in the Catalan territories, Endemixit in Italy, Norwegian Earth Biogenome Project, and SciLifeLab in Sweden, on applications such as the LOEWE Translational Biodiversity Genomics in Germany, or on ecological systems such as the Aquatic Symbiosis Genomics project. Collectively part of the Earth BioGenome Project (EBP), in Europe these initiatives are organized under the umbrella of the European Reference Genome Atlas (ERGA). A genome atlas of European biodiversityERGA is a pan-European scientific response to the current threats to biodiversity. Approximately one fifth of the ~200 000 eukaryotic species present in Europe can be inferred to be at risk of extinction according to the International Union for Conservation of Nature (IUCN) Red List classification (this estimate only considers the assessed species; https://www.iucn.org/regions/europe/our-work/biodiversity-conservation/european-red-list-threatened-species).ERGA aims to generate reference genomes of European eukaryotic species across the tree of life, including threatened, endemic, and keystone species, as well as pests and species important to agriculture, fisheries, and ecosystem function and stability. ERGA builds upon current genomic consortia in EU member states, EU Associated Countries, representatives of other countries within the European bioregion, and international collaborators. These reference genomes will address fundamental and applied questions in conservation, biology, and health. ERGA seeks to alert the EU about the potential of conservation genomics, and particularly the role of reference genomes, in biodiversity assessment, conservation strategies, and restoration efforts.
Hybridization is continually documented in primates, but effects of natural and anthropogenic hybridization on biodiversity are still unclear and differentiating between these contexts remains challenging in regards to primate evolution and conservation. Here, we examine hybridization effects on the mitochondrial DNA (mtDNA) control region of Callithrix marmosets, which provide a unique glimpse into interspecific mating under distinct anthropogenic and natural conditions. DNA was sampled from 40 marmosets along a 50-km transect from a previously uncharacterized hybrid zone in NE Brazil between the ranges of Callithrix jacchus and Callithrix penicillata. DNA was also collected from 46 marmosets along a 30-km transect in a hybrid zone in Rio de Janeiro state, Brazil, where exotic marmosets appeared in the 1980s. Combining Callithrix DNA sampled inside and outside of these hybrid zones, phylogenetic and network analyses show C. jacchus and C. penicillata being parental species to sampled hybrids. We expand limited Callithrix population genetics work by describing mtDNA diversity and demographic history of these parental species. We show ancient population expansion in C. jacchus and historically constant population size in C. penicillata, with the latter being more genetically diverse than the former. The natural hybrid zone contained higher genetic diversity relative to the anthropogenic zone. While our data suggest hybrid swarm formation within the anthropogenic zone due to removed physical reproductive barriers, this pattern is not seen in the natural hybrid zone. These results suggest different genetic dynamics within natural and anthropogenic hybridization contexts that carry important implications for primate evolution and conservation.
Background Callithrix marmosets are a relatively young primate radiation, whose phylogeny is not yet fully resolved. These primates are naturally para- and allopatric, but three species with highly invasive potential have been introduced into the southeastern Brazilian Atlantic Forest by the pet trade. There, these species hybridize with each other and endangered, native congeners. We aimed here to reconstruct a robust Callithrix phylogeny and divergence time estimates, and identify the biogeographic origins of autochthonous and allochthonous Callithrix mitogenome lineages. We sequenced 49 mitogenomes from four species (C. aurita, C. geoffroyi, C. jacchus, C. penicillata) and anthropogenic hybrids (C. aurita x Callithrix sp., C. penicillata x C. jacchus, Callithrix sp. x Callithrix sp., C. penicillata x C. geoffroyi) via Sanger and whole genome sequencing. We combined these data with previously published Callithrix mitogenomes to analyze five Callithrix species in total. Results We report the complete sequence and organization of the C. aurita mitogenome. Phylogenetic analyses showed that C. aurita was the first to diverge within Callithrix 3.54 million years ago (Ma), while C. jacchus and C. penicillata lineages diverged most recently 0.5 Ma as sister clades. MtDNA clades of C. aurita, C. geoffroyi, and C. penicillata show intraspecific geographic structure, but C. penicillata clades appear polyphyletic. Hybrids, which were identified by phenotype, possessed mainly C. penicillata or C. jacchus mtDNA haplotypes. The biogeographic origins of mtDNA haplotypes from hybrid and allochthonous Callithrix were broadly distributed across natural Callithrix ranges. Our phylogenetic results also evidence introgression of C. jacchus mtDNA into C. aurita. Conclusion Our robust Callithrix mitogenome phylogeny shows C. aurita lineages as basal and C. jacchus lineages among the most recent within Callithrix. We provide the first evidence that parental mtDNA lineages of anthropogenic hybrid and allochthonous marmosets are broadly distributed inside and outside of the Atlantic Forest. We also show evidence of cryptic hybridization between allochthonous Callithrix and autochthonous C. aurita. Our results encouragingly show that further development of genomic resources will allow to more clearly elucidate Callithrix evolutionary relationships and understand the dynamics of Callithrix anthropogenic introductions into the Brazilian Atlantic Forest.
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