Uniparental genetic markers to investigate hybridization in wild-born marmosets with a mixed phenotype among Callithrix aurita and invasive species

Denise Monnerat Nogueira,Helena Godoy Bergallo,Daniel Gomes Pereira,Thiago Silva De Paula,Silvia De Oliveira Loiola,Elizeu Fagundes Carvalho,Alcides Pissinatti,Andréa Maria De Oliveira,Dayse Aparecida Silva,Ana Maria Dos Reis Ferreira,Rodrigo Salles De Carvalho

doi:10.1038/s41598-021-04276-7

Abstract

The native marmoset of the Southeastern Atlantic Forest in Brazil is among the 25 most endangered primates of the world. Hybridization with alien species is one of its main threats registered since the early 2000s based on phenotype, so far, without genetic confirmation. Using uniparental molecular markers, we analyzed 18 putative hybrids, captured from 2004 to 2013 in different localities of the Atlantic Forest. A nine base pair deletion in the SRY gene of C. aurita was used to investigate paternal ancestry. Maternal ancestry was assessed by DNA sequencing of ca. 455 bp from the COX2 gene. Hybridization was confirmed for 16 out of the 18 marmosets since they inherited COX2 haplotypes of the alien C. penicillata or C. jacchus and the SRY deletion specific to C. aurita. Two individuals inherited both parental lineages of C. aurita, which is probably related to backcrossing or hybrid interbreeding. The direction of hybridization of females with the matrilineal lineage of invasive species with males descending from the native lineage was predominant in our sampling. This is the first time that hybridization between C. aurita and invasive species has been confirmed through genetic analysis.

Highlights

The native marmoset of the Southeastern Atlantic Forest in Brazil is among the 25 most endangered primates of the world
The color of the body was lighter with eventual grooves (Fig. 2). These features confer to the individuals sampled a mixed pelage pattern of the tufts and the back, suggesting that they are hybrids between C. aurita and C. penicillata or C. jacchus[29,32,41]
The hybrids sampled were distributed throughout the original area of occurrence of C. aurita, with one locality in São Paulo state at Biritiba Mirim and three localities of Rio de Janeiro state, in the municipalities of Teresópolis, Guapimirim and Petrópolis

Summary

Introduction

The native marmoset of the Southeastern Atlantic Forest in Brazil is among the 25 most endangered primates of the world. The buffy-tufted-ear marmoset, Callithrix aurita is endemic to the Brazilian Atlantic Forest, occurring in the states of Rio de Janeiro, eastern and northeastern São Paulo and adjacent parts of Minas Gerais. In contrast to C. aurita, both species are generalists and inhabitants of secondary forests, which putatively enable them to have a greater degree of environmental plasticity to adapt to degraded areas and expand their territories[15,16] These two species hybridize naturally in a contact zone of their original range in the northeast and by human-mediated introduction in Rio de Janeiro s tate[13]. At the species taxonomic level, it results in progeny that carry a mixture of previously isolated gene pools It occurs naturally at distribution boundaries between closely related species in hybrid zones that act as a "filter testing new genotypic combinations through natural selection”[18]. It is estimated to occur naturally in more than 10% of primate s pecies[18]

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Conclusion