Hybridization effects and genetic diversity of the common and black‐tufted marmoset (Callithrix jacchusandCallithrix penicillata) mitochondrial control region

Abstract

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.

Phylogeny of the jacchus group of Callithrix marmosets based on complete mitochondrial genomes

“…Skin tissue samples were generously donated by Dr. Jeffrey French from the Callitrichid Research Center (CRC) at the University of Nebraska Omaha. These tissues were collected from captive marmoset populations for other projects under the approval of the Arizona State University Institutional Animal Care and Use Committee Animals (ASU IACUC, protocol #11‐1150R), and sample collection details are given in Malukiewicz et al (). Source tissue species assignments were based on CRC records, animal phenotypes, and were genetically confirmed in Malukiewicz et al ().…”

“…These tissues were collected from captive marmoset populations for other projects under the approval of the Arizona State University Institutional Animal Care and Use Committee Animals (ASU IACUC, protocol #11‐1150R), and sample collection details are given in Malukiewicz et al (). Source tissue species assignments were based on CRC records, animal phenotypes, and were genetically confirmed in Malukiewicz et al (). We used DNA samples from one female C. kuhlii , one male C. geoffroyi , one female C. jacchus , and one female C. penicillata (Table ).…”

“…Additionally, Malukiewicz et al () produced a phylogeny of C. aurita and the jacchus group based on a larger number of Callithrix D‐loop haplotypes than that of Tagliaro et al () ‐ 176 for the former vs. 15 for the latter. However, in their phylogeny, C. geoffroyi was sister all other species including C. aurita , and C. kuhlii and C. penicillata were polyphyletic (Malukiewicz et al, ), likely due to incomplete sorting of Callithrix mitochondrial lineages (Funk & Omland, ; Malukiewicz et al, ). The difficulty of investigating the evolutionary relationships among members of the jacchus group may partially be due to the relatively young age of the Callithrix genus, estimated to be approximately 2.5 million years old (Perelman et al, ).…”

Morphological and genetic diversity in Callithrix hybrids in an anthropogenic area in southeastern Brazil (Primates: Cebidae: Callitrichinae)

“…Malukiewicz et al (2014) agreed that the current situation of coastal lowland marmosets is the result of multiple introductions and that there some new genetic variations caused by new introductions. These multiple introductions may not only be from pure parental individuals but also from hybrid individuals, resulting in crosses between pure and mixed ancestries that give rise to highly variable phenotypes.…”

“…They are phylogenetically very close, and it has been hypothesized that their most recent common ancestor lived about 700 thousand years ago, in the Atlantic Forest, Cerrado, and Caatinga. A subsequent vicariant speciation event isolated the ancestor of C. penicillata in the Cerrado or Caatinga (Buckner et al, 2014Malukiewicz et al 2014.…”