Reticulate evolutionary history and extensive introgression in mosquito species revealed by phylogenetic network analysis

Abstract

The role of hybridization and subsequent introgression has been demonstrated in an increasing number of species. Recently, Fontaine et al. (Science, 347, 2015, 1258524) conducted a phylogenomic analysis of six members of the Anopheles gambiae species complex. Their analysis revealed a reticulate evolutionary history and pointed to extensive introgression on all four autosomal arms. The study further highlighted the complex evolutionary signals that the co-occurrence of incomplete lineage sorting (ILS) and introgression can give rise to in phylogenomic analyses. While tree-based methodologies were used in the study, phylogenetic networks provide a more natural model to capture reticulate evolutionary histories. In this work, we reanalyse the Anopheles data using a recently devised framework that combines the multispecies coalescent with phylogenetic networks. This framework allows us to capture ILS and introgression simultaneously, and forms the basis for statistical methods for inferring reticulate evolutionary histories. The new analysis reveals a phylogenetic network with multiple hybridization events, some of which differ from those reported in the original study. To elucidate the extent and patterns of introgression across the genome, we devise a new method that quantifies the use of reticulation branches in the phylogenetic network by each genomic region. Applying the method to the mosquito data set reveals the evolutionary history of all the chromosomes. This study highlights the utility of ‘network thinking’ and the new insights it can uncover, in particular in phylogenomic analyses of large data sets with extensive gene tree incongruence.

Hybridization in Plants: Old Ideas, New Techniques

“…These methods are computationally demanding and make controversial evolutionary assumptions (Sousa and Hey, 2013;Payseur and Rieseberg, 2016). Models of phylogenetic networks (Than et al, 2008;Solís-Lemus and Ané, 2016;Wen et al, 2016) and the five-taxa extension of the ABBA-BABA test (Eaton and Ree, 2013;Pease and Hahn, 2015) have made progress toward evaluating the direction and magnitude of introgression, and future efforts should continue to develop such methods.…”

Bayesian Inference Of Phylogenetic Networks From Bi-allelic Genetic Markers

“…Horizontal gene transfer is ubiquitous in 71 prokaryotes [9,10], and several bodies of work are pointing to much larger extent and 72 role of hybridization in eukaryotic evolution than once thought [8,[11][12][13][14][15]. Not only does 73 hybridization play an important role in the genomic diversification of several eukaryotic 74 groups, but increasing evidence is pointing to the adaptive role it has played, for 75 example, in wild sunflowers [16], humans [17], macaques [18], mice [19], butterflies [20], 76 and mosquitoes [21,22].…”

Phylogenetics, Reticulation and Evolution

“…This has been recently demonstrated in extant Anopheles mosquitoes [15] and in some Heliconius buterly species and to detect past hybridization events using ancient DNA [16]. These instances force us to accept an ad hoc species deinition applicable only to terminal taxa, rather than to the original bifurcating ancestors.…”

“…Recent indings of shared polymorphisms between them include the MHC and ABO blood group loci. In the species complex of Anopheles gambiae, a very large chromosomal inversion encompassing 8.5% of its genome size is maintained by a balanced selection-driven populational regime [15]. Unlike lateral transfer and introgression, incomplete lineage sorting does not result in phylogenetic reticulation at species level.…”