Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys

Abstract

Background: Colobine 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.

Results: Gene 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.

Conclusions: Overall, 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.

Figure 1

Phylogenetic relationships among colobine and outgroup genera as inferred from different datasets. Panels refer to insertions of mobile elements (A), combined nuclear sequence data (B), and mitochondrial genome data (C). Roman numbers are used as branch identifiers and are discussed in the text. In A, numbers in flags represent the number of available mobile elements (black: colobine markers, grey: non-colobine markers). In B and C, all nodes are significantly supported by ML and Bayesian reconstructions (≥95%, 1.0). Black and grey dots on nodes indicate high (≥95%) and lower (<95%) branch support as obtained from MP (in A-C) and NJ (in B and C) reconstructions, respectively. Bootstrap values <95% are presented at respective nodes. In C, first and second values refer to those obtained from reconstructions using datasets mtDNA1 and mtDNA2, respectively.

Figure 2

The nine alternative hybridization scenarios compared in the coalescent framework. Beneath each tree, the number of parameters in the model (k) is given as well as the AIC. The lowest AIC values are observed for trees F and I, which indicate a similar fit for these scenarios.

Figure 3

Dispersal scenario for colobine monkeys. Colobines most likely originated in western Africa. After the successive split of Colobus (~10.9 mya) and a progenitor of Piliocolobus/Procolobus (~10.7 mya) from the ancestor of Asian colobines, gene flow between both African lineages via female introgression from the Piliocolobus/Procolobus progenitor into Colobus occurred until ~8.5 mya (displayed by red-dashed arrow). During the late Miocene, colobines invaded eastern Asia most likely via a route north of the Himalayas. After their arrival at the Hengduan Mountains, Asian colobines diversified into a lineage comprising a progenitor of the odd-nosed monkeys and Trachypithecus/Presbytis, and of Semnopithecus, which later colonized the Indian subcontinent. Shortly afterwards, Trachypithecus/Presbytis split off from odd-nosed monkeys, and migrated to southern mainland Asia, before finally both genera diverged from each other. In the region of today's Burma, Bangladesh and India, Semnopithecus and Trachypithecus came into secondary contact and hybridized until ~2.6 mya (displayed by red-dashed arrow). In the latest Miocene, odd-nosed monkeys migrated from China to the south and expanded their range into Indochina and Sundaland. Nasalis and Simias finally separated from each other 1.1-1.9 mya.