Genetic diversity in two sibling species of the Anopheles punctulatus group of mosquitoes on Guadalcanal in the Solomon Islands

Abstract

Background: The mosquito Anopheles irenicus, a member of the Anopheles punctulatus group, is geographically restricted to Guadalcanal in the Solomon Islands. It shows remarkable morphological similarities to one of its sibling species, An. farauti sensu stricto (An. farauti s.s.), but is dissimilar in host and habitat preferences. To infer the genetic variations between these two species, we have analyzed mitochondrial cytochrome oxidase subunit II (COII) and nuclear ribosomal internal transcribed spacer 2 (ITS2) sequences from Guadalcanal and from one of its nearest neighbours, Malaita, in the Solomon Islands.

Results: An. farauti s.s. was collected mostly from brackish water and by the human bait method on both islands, whereas An. irenicus was only collected from fresh water bodies on Guadalcanal Island. An. irenicus is distributed evenly with An. farauti s.s. (Phi SC = 0.033, 0.38%) and its range overlaps in three of the seven sampling sites. However, there is a significant population genetic structure between the species (Phi CT = 0.863, P < 0.01; Phi ST = 0.865, P < 0.01 and FST = 0.878, P < 0.01). Phylogenetic analyses suggest that An. irenicus is a monophyletic species, not a hybrid, and is closely related to the An. farauti s.s. on Guadalcanal. The time estimator suggests that An. irenicus diverged from the ancestral An. farauti s.s. on Guadalcanal within 29,000 years before present (BP). An. farauti s.s. expanded much earlier on Malaita (texp = 24,600 BP) than the populations on Guadalcanal (texp = 16,800 BP for An. farauti s.s. and 14,000 BP for An. irenicus).

Conclusion: These findings suggest that An. irenicus and An. farauti s.s. are monophyletic sister species living in sympatry, and their populations on Guadalcanal have recently expanded. Consequently, the findings further suggest that An. irenicus diverged from the ancestral An. farauti s.s. on Guadalcanal.

Figure 1

Collection sites and frequencies of Anopheles farauti s.s. and Anopheles irenicus mosquitoes used in this study. Dots indicate several nearer sampling sites. Pie charts represent the proportion of species collected from each site. Inset: The study area within Melanesia is shown.

Figure 2

Maximum Parsimony (MP) consensus tree for 684 bp COII haplotypes in mitochondrial DNA using the GTR+I+G model. The trees were rooted with D. melanogaster and Bi. hollandi. Bootstrap values of > 90% are shown above the branch in italics and posterior probability values of > 0.75 are shown below the branch. S and I indicate haplotypes of An. farauti s.s. of the Solomon Islands and An. irenicus, respectively. Collection sites are represented after haplotypes where sampled from multiple sites. G, Guadalcanal; M, Malaita; SI, Solomon Islands; PNG, Papua New Guinea; Van, Vanuatu Islands. Sample codes and GenBank accession number for each specimen are given in [additional file 1].

Figure 3

Maximum Parsimony (MP) consensus tree for 760 bp ITS2 haplotypes in nuclear ribosomal DNA using the HKY85+G model. The trees were rooted with An. koliensis. Bootstrap values of > 90% are shown above the branch in italics and posterior probability values of > 0.90 are shown below the branch. S1 and I1 indicate haplotypes of An. farauti s.s. of the Solomon Islands and An. irenicus, respectively. For species collected from multiple sites, species names are followed by localities. AUS, Australia; PNG, Papua New Guinea; SI, Solomon Islands; Van, the Vanuatu Islands; G, Guadalcanal; N, northern part; S, southern part; Rab, Rabaul; Q, Queensland. Sample codes and GenBank accession number for each specimen are given in [additional file 1].