Population structure, mitochondrial polyphyly and the repeated loss of human biting ability in anopheline mosquitoes from the southwest Pacific

Abstract

Australia and New Guinea contain high levels of endemism and biodiversity, yet there have been few evaluations of population-level genetic diversity in fauna occurring throughout the Australo-Papuan region. Using extensive geographical sampling, we examined and compared the phylogenetic relationships, phylogeography and population structure of Anopheles farauti, An. hinesorum and An. irenicus throughout their ranges in the southwest Pacific using mitochondrial (mtDNA COI) and nuclear (ribosomal protein S9 and ribosomal DNA ITS2) loci. Phylogenetic analyses suggest that the ability to utilize humans as hosts has been lost repeatedly, coincident with independent colonizations of the Solomon Islands. As some of the species under investigation transmit malaria in the region, this is a medically important finding. Maximum likelihood and Bayesian phylogenetic analyses of nuclear loci also showed that the three species are monophyletic. However, putative introgression of An. hinesorum mtDNA onto a nuclear background of An. farauti was evident in populations from Queensland, Torres Strait and southern New Guinea. Haplotype networks and pairwise FST values show that there is significant genetic structure within New Guinea and Australia in both An. farauti and An. hinesorum, consistent with a long-term history of low gene flow among populations.

Mitochondrial genome sequences reveal deep divergences among Anopheles punctulatus sibling species in Papua New Guinea

“…farauti s.s. and An . hinesorum , are similar to those of previous studies [11,28,37]. When the estimated mutation rate for insect mtDNA was used [52], the divergence dates obtained were significantly younger than those obtained using a calibration point [see Additional file 5].…”

“…This study suggests that the different AP sibling species diverged from each other 25–54 mya, much earlier than proposed in previous studies of the AP group [26,28]. This deep divergence among AP mosquitoes is unlikely to be caused by a single species that could have diverged from the other sibling species in SEA and colonized PNG later.…”

“…gambiae being too divergent), the high divergence among AP species at the nuclear level and the high level of genetic diversity within species. However, there is little evidence of gene flow among AP mosquitoes (but see also Ambrose [28]) and early forced mating studies suggested that most hybrids are non-viable or sterile [15]. Overall, these observations suggest that, for this dataset, the mt gene tree likely recapitulates the actual species tree.…”

“…This mutation rate, while widely used (see e.g. [28]) was originally calculated using closely related species (the maximum divergence time used in the study was ~3 mya) and, Brower noted, probably overestimated the actual mutation rate. A slower mutation rate would push estimated divergence dates back in time, closer to the estimates obtained using calibration points.…”

“…farauti 4 - have been described as competent vectors of malaria [23,24]. Phylogenetic studies of this group have focused on DNA sequences of ribosomal RNAs [25,26], mitochondrial genes [27,28], ribosomal ITS2 [19], and voltage-gated sodium channel gene [29]. However, the genetic information generated in these studies has not allowed robust determination of the AP group phylogeny and has often yielded conflicting results [19,27].…”