Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys

Abstract

BackgroundColobine monkeys constitute a diverse group of primates with major radiations in Africa and Asia. However, phylogenetic relationships among genera are under debate, and recent molecular studies with incomplete taxon-sampling revealed discordant gene trees. To solve the evolutionary history of colobine genera and to determine causes for possible gene tree incongruences, we combined presence/absence analysis of mobile elements with autosomal, X chromosomal, Y chromosomal and mitochondrial sequence data from all recognized colobine genera.ResultsGene tree topologies and divergence age estimates derived from different markers were similar, but differed in placing Piliocolobus/Procolobus and langur genera among colobines. Although insufficient data, homoplasy and incomplete lineage sorting might all have contributed to the discordance among gene trees, hybridization is favored as the main cause of the observed discordance. We propose that African colobines are paraphyletic, but might later have experienced female introgression from Piliocolobus/Procolobus into Colobus. In the late Miocene, colobines invaded Eurasia and diversified into several lineages. Among Asian colobines, Semnopithecus diverged first, indicating langur paraphyly. However, unidirectional gene flow from Semnopithecus into Trachypithecus via male introgression followed by nuclear swamping might have occurred until the earliest Pleistocene.ConclusionsOverall, our study provides the most comprehensive view on colobine evolution to date and emphasizes that analyses of various molecular markers, such as mobile elements and sequence data from multiple loci, are crucial to better understand evolutionary relationships and to trace hybridization events. Our results also suggest that sex-specific dispersal patterns, promoted by a respective social organization of the species involved, can result in different hybridization scenarios.

Summary of phylogeny in subfamily Colobinae (Primate: Cercopithecidae)

“…Interestingly, a recent phylogenetic analyses of 83 mobile elements from Roos et al [19] indicated a closer association of the Procolobus/Piliocolobus clade to Asian colobines than to Colobus, a relationship that was not rejected by nuclear sequence data in their study, leading them to propose African colobines paraphyly hypothesis ( Figure 3(e)). This finding thus challenged the traditional view of the monophyly of African colobines.…”

“…In earlier analyses of morphological and molecular data, all supported that the African colobine forms a monophyletic clade [1,12,19], grouping Piliocolobus, Procolobus, and Colobus together [17][18][19][24][25][26]29,30] (Figure 3). Interestingly, a recent phylogenetic analyses of 83 mobile elements from Roos et al [19] indicated a closer association of the Procolobus/Piliocolobus clade to Asian colobines than to Colobus, a relationship that was not rejected by nuclear sequence data in their study, leading them to propose African colobines paraphyly hypothesis ( Figure 3(e)).…”

“…Colobus diverged first, and followed by the progenitor of Piliocolobus and Procolobus [17,19,[24][25][26]. Based on both morphology and genetics evidence, it was well-recognized that Procolobus was the sister-taxon of (and possibly congeneric to) Piliocolobus [12,19,24,[26][27][28].…”

“…In comparison, Figure 3 Hypotheses of phylogenetic relationships among Colobine genera. Trees were reconstructed based on (a) 12 protein-coding mt genes (10 kb) [17]; (b) fragment of X-chromosome (4.3 kb) [26] and 54 nuclear genes (35 kb) [18]; (c) complete cytb gene (1.8 kb) [30] and 7 mt genes (6.1 kb) [29]; (d) 15 mt genes and 43 nuclear genes (42 kb) [25], 44 nuclear non-coding genes (23 kb) [31]; (e) 83 mobile elements [19]; (f) nuclear genes (13 kb) [19]; (g) complete mt genomes (16.5 kb) [31].…”

“…Understanding the true evolutionary history of the colobine monkeys, therefore, becomes an important field and has received special attention. However, due to the fact that nearly all the extant colobine genera diversify from one another within a four-million-year window [17][18][19], attempts to clarify relationships among these colobine genera have encountered challenges.…”