Alu insertion polymorphisms shared by Papio baboons and Theropithecus gelada reveal an intertwined common ancestry

Abstract

BackgroundBaboons (genus Papio) and geladas (Theropithecus gelada) are now generally recognized as close phylogenetic relatives, though morphologically quite distinct and generally classified in separate genera. Primate specific Alu retrotransposons are well-established genomic markers for the study of phylogenetic and population genetic relationships. We previously reported a computational reconstruction of Papio phylogeny using large-scale whole genome sequence (WGS) analysis of Alu insertion polymorphisms. Recently, high coverage WGS was generated for Theropithecus gelada. The objective of this study was to apply the high-throughput “poly-Detect” method to computationally determine the number of Alu insertion polymorphisms shared by T. gelada and Papio, and vice versa, by each individual Papio species and T. gelada. Secondly, we performed locus-specific polymerase chain reaction (PCR) assays on a diverse DNA panel to complement the computational data.ResultsWe identified 27,700 Alu insertions from T. gelada WGS that were also present among six Papio species, with nearly half (12,956) remaining unfixed among 12 Papio individuals. Similarly, each of the six Papio species had species-indicative Alu insertions that were also present in T. gelada. In general, P. kindae shared more insertion polymorphisms with T. gelada than did any of the other five Papio species. PCR-based genotype data provided additional support for the computational findings.ConclusionsOur discovery that several thousand Alu insertion polymorphisms are shared by T. gelada and Papio baboons suggests a much more permeable reproductive barrier between the two genera then previously suspected. Their intertwined evolution likely involves a long history of admixture, gene flow and incomplete lineage sorting.

Insertion of Telomeric Repeats in the Human and Horse Genomes: An Evolutionary Perspective

“…It is well-known that insertion sequences that were introduced recently during evolution can display insertion polymorphism [36][37][38][39][40][41][42]49,50]. That is to say that the insertion-containing allele is not yet fixed, and the empty ancestral allele is also present in the population.…”

“…That is to say that the insertion-containing allele is not yet fixed, and the empty ancestral allele is also present in the population. Sequences showing insertion polymorphism have been used as markers for population genetic studies in many species including humans [37,42,47,49] and, in some cases, they have been associated to gene expression regulation [43,49]. To our knowledge, insertion polymorphism at short-ITS loci has not been described so far.…”

“…Since ITS loci originated from the insertion of a telomeric repeat stretch at a DNA double-strand break site during evolution, we might expect that, for recently inserted ITS loci, empty ITS-less alleles are found in the same species, generating insertion polymorphism. Several studies demonstrated that transposable elements, such as Alu retrotransposons in humans, are characterized by insertion polymorphism [36][37][38][39][40][41][42]. This type of transposable element polymorphism can be involved in gene expression modulation leading to phenotypic consequences [43], including human and animal disease [44,45], and can be particularly informative for population genetics studies [46][47][48].…”

Hybrid apes in the Anthropocene: Burden or asset for conservation?

“…In baboons (Papio spp. ), some populations consist of >30% hybrid individuals (Ackermann et al, 2006), and cross-breeding may even happen with distinct genera (Rungwecebus, Theropithecus; Walker et al, 2019;Zinner et al, 2009). Consequently, hybridisation is not only quite common, but often advantageous for survival, breeding and speciation.…”

Baboon biogeography, divergence, and evolution: Morphological and paleoecological perspectives

“…Relationships within the clade are far from clear cut (Liedigk et al, 2014). On balance, Theropithecus is most likely to be sister to a Lophocebus / Papio clade (Harris, 2000;Guevara and Steiper, 2014), although Theropithecus and Lophocebus may have continued to hybridise after the initial split (Guevara and Steiper, 2014), and there is also mounting evidence for introgression, potentially over a long period, between Theropithecus and Papio (Walker et al, 2019). Introgression between Rungwecebus and Papio is certain (Burrell et al, 2009;Zinner et al, 2009bZinner et al, , 2018Roberts et al, 2010), with Papio mtDNA introgression in the Mount Rungwe Rungwecebus population and vice versa in the Udzungwa Mountains (Zinner et al, 2018).…”