Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa

Abstract

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.

Genomic Skimming and Nanopore Sequencing Uncover Cryptic Hybridization in One of World’s Most Threatened Primates

“…In our phylogeny, the mitogenomic lineage of individual BJT022 unexpectedly clustered not within the C. aurita clade, but rather with the C. penicillata Caatinga clade. Additionally, two mitogenome lineages from the Malukiewicz et al (2021) 7 study that originated from two marmosets with C. aurita phenotypes clustered within the C. jacchus clade in the previous phylogeny as well as in ours. Thus, these two studies show three cases of cryptic marmosets hybrids with discordant C. aurita phenotypes and non-C. aurita mitogenomic lineages.…”

“…Zoological records state that the individual originates from São Jose dos Campos, SP (Figure 1). Based on previous phenotypic and morphological description of the species 7,8,17 , we initially identified the individual as C. aurita. The individual had the yellow ear tufts characteristic of C. aurita, as well as yellow pelage above the forehead, and other yellow patches around the facial region 17 .…”

“…We used Callithrix mitogenome sequences from Malukiewicz et al (2021) 7 to calculate diversity indexes of four Callithrix species (C. aurita, C. jacchus, C. geoffroyi, and C. penicillata), for which haplotypes were available for three or more individuals per species (Table 4). Relative to the other four species, C. penicillata showed much higher values across all diversity indexes (Table 4).…”

“…In this work, we aimed to develop a rapid, cost-effective protocol to obtain genomic data for one of the world's most endangered primates, the small buffy-tufted-ear marmoset C. aurita (Figure 1), for which there is relatively little genetic knowledge. This species is native to the mountainous regions of southeastern Brazil 6,7,8 , and there are about 10,000 mature C. aurita remaining in the wild 9 . The IUCN Red List considers this species Endangered, and C. aurita conservation threats include habitat deforestation, urbanization, and logging 9 .…”

“…The IUCN Red List considers this species Endangered, and C. aurita conservation threats include habitat deforestation, urbanization, and logging 9 . The buffy-tufted-ear marmoset also faces ecological and hybridization threats from two invasive marmoset species that have been introduced by humans into southeastern Brazil, C. jacchus and C. penicillata (natural ranges and species shown in Figure 1) 7,8,9,10,11 . Currently, a captive breeding program is underway for C. aurita, with the aim to eventually reintroduce the species into the wild.…”