skip to main content


Title: Phylogenomics reveals the history of host use in mosquitoes
Abstract

Mosquitoes have profoundly affected human history and continue to threaten human health through the transmission of a diverse array of pathogens. The phylogeny of mosquitoes has remained poorly characterized due to difficulty in taxonomic sampling and limited availability of genomic data beyond the most important vector species. Here, we used phylogenomic analysis of 709 single copy ortholog groups from 256 mosquito species to produce a strongly supported phylogeny that resolves the position of the major disease vector species and the major mosquito lineages. Our analyses support an origin of mosquitoes in the early Triassic (217 MYA [highest posterior density region: 188–250 MYA]), considerably older than previous estimates. Moreover, we utilize an extensive database of host associations for mosquitoes to show that mosquitoes have shifted to feeding upon the blood of mammals numerous times, and that mosquito diversification and host-use patterns within major lineages appear to coincide in earth history both with major continental drift events and with the diversification of vertebrate classes.

 
more » « less
Award ID(s):
1754376
NSF-PAR ID:
10467983
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; « less
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Volume:
14
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Aedes aegyptiis among the best‐studied mosquitoes due to its critical role as a vector of human pathogens and ease of laboratory rearing. Until now, this species was thought to have originated in continental Africa, and subsequently colonized much of the world following the establishment of global trade routes. However, populations of this mosquito on the islands in the southwestern Indian Ocean (SWIO), where the species occurs with its nearest relatives referred to as the Aegypti Group, have received little study. We re‐evaluated the evolutionary history ofAe. aegyptiand these relatives, using three data sets: nucleotide sequence data, 18,489 SNPs and 12 microsatellites. We found that: (a) the Aegypti Group diverged 16 MYA (95% HPD: 7–28 MYA) from its nearest African/Asian ancestor; (b) SWIO populations ofAe. aegyptiare basal to continental African populations; (c) after diverging 7 MYA (95% HPD: 4–15 MYA) from its nearest formally described relative (Ae. mascarensis),Ae. aegyptimoved to continental Africa less than 85,000 years ago, where it recently (<1,000 years ago) split into two recognized subspeciesAe. aegypti formosusand a human commensal,Ae. aegypti aegypti; (d) the Madagascar samples form a clade more distant from all otherAe. aegyptithan the named speciesAe. mascarensis, implying that Madagascar may harbour a new cryptic species; and (e) there is evidence of introgression betweenAe. mascarensisandAe. aegyption Réunion, and between the two subspecies elsewhere in the SWIO, a likely consequence of recent introductions of domesticAe. aegypti aegyptifrom Asia.

     
    more » « less
  2. null (Ed.)
    Advances in genomics have led to an appreciation that introgression is common, but its evolutionary consequences are poorly understood. In recent species radiations the sharing of genetic variation across porous species boundaries can facilitate adaptation to new environments and generate novel phenotypes, which may contribute to further diversification. Most Anopheles mosquito species that are of major importance as human malaria vectors have evolved within recent and rapid radiations of largely nonvector species. Here, we focus on one of the most medically important yet understudied anopheline radiations, the Afrotropical Anopheles funestus complex (AFC), to investigate the role of introgression in its diversification and the possible link between introgression and vector potential. The AFC comprises at least seven morphologically similar species, yet only An. funestus sensu stricto is a highly efficient malaria vector with a pan-African distribution. Based on de novo genome assemblies and additional whole-genome resequencing, we use phylogenomic and population genomic analyses to establish species relationships. We show that extensive interspecific gene flow involving multiple species pairs has shaped the evolutionary history of the AFC since its diversification. The most recent introgression event involved a massive and asymmetrical movement of genes from a distantly related AFC lineage into An. funestus , an event that predated and plausibly facilitated its subsequent dramatic geographic range expansion across most of tropical Africa. We propose that introgression may be a common mechanism facilitating adaptation to new environments and enhancing vectorial capacity in Anopheles mosquitoes. 
    more » « less
  3. Abstract

    Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto‐predaceousLepidochrysopsbutterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time‐calibrated phylogeny forLepidochrysopsand its closest, non‐parasitic relatives in theEuchrysopssection (Poloyommatini). We estimated ancestral areas across the phylogeny with process‐based biogeographical models and diversification rates relying on time‐variable and clade‐heterogeneous birth‐death models. TheEuchrysopssection originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non‐parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto‐predaceousLepidochrysopslineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of theEuchrysopssection, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto‐predaceous life history in species ofLepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.

     
    more » « less
  4. Abstract Background

    West Nile virus (WNV), primarily vectored by mosquitoes of the genusCulex, is the most important mosquito-borne pathogen in North America, having infected thousands of humans and countless wildlife since its arrival in the USA in 1999. In locations with dedicated mosquito control programs, surveillance methods often rely on frequent testing of mosquitoes collected in a network of gravid traps (GTs) and CO2-baited light traps (LTs). Traps specifically targeting oviposition-seeking (e.g. GTs) and host-seeking (e.g. LTs) mosquitoes are vulnerable to trap bias, and captured specimens are often damaged, making morphological identification difficult.

    Methods

    This study leverages an alternative mosquito collection method, the human landing catch (HLC), as a means to compare sampling of potential WNV vectors to traditional trapping methods. Human collectors exposed one limb for 15 min at crepuscular periods (5:00–8:30 am and 6:00–9:30 pm daily, the time whenCulexspecies are most actively host-seeking) at each of 55 study sites in suburban Chicago, Illinois, for two summers (2018 and 2019).

    Results

    A total of 223 human-seeking mosquitoes were caught by HLC, of which 46 (20.6%) were mosquitoes of genusCulex. Of these 46 collectedCulexspecimens, 34 (73.9%) wereCx. salinarius, a potential WNV vector species not thought to be highly abundant in upper Midwest USA. Per trapping effort, GTs and LTs collected > 7.5-fold the number of individualCulexspecimens than HLC efforts.

    Conclusions

    The less commonly used HLC method provides important insight into the complement of human-biting mosquitoes in a region with consistent WNV epidemics. This study underscores the value of the HLC collection method as a complementary tool for surveillance to aid in WNV vector species characterization. However, given the added risk to the collector, novel mitigation methods or alternative approaches must be explored to incorporate HLC collections safely and strategically into control programs.

    Graphical Abstract 
    more » « less
  5. Abstract

    The Great American Biotic Interchange (GABI) was a key biogeographic event in the history of the Americas. The rising of the Panamanian land bridge ended the isolation of South America and ushered in a period of dispersal, mass extinction, and new community assemblages, which sparked competition, adaptation, and speciation. Diversification across many bird groups, and the elevational zonation of others, ties back to events triggered by the GABI. But the exact timing of these events is still being revealed, with recent studies suggesting a much earlier time window for faunal exchange, perhaps as early as 20 million years ago (Mya). Using a time‐calibrated phylogenetic tree, we show that the jay genusCyanolycais emblematic of bird dispersal trends, with an early, pre‐land bridge dispersal from Mesoamerica to South America 6.3–7.3 Mya, followed by a back‐colonization ofC. cucullatato Mesoamerica 2.3–4.8 Mya, likely after the land bridge was complete. AsCyanolycaspecies came into contact in Mesoamerica, they avoided competition due to a prior shift to lower elevation in the ancestor ofC. cucullata. This shift allowedC. cucullatato integrate itself into the Mesoamerican highland avifauna, which our time‐calibrated phylogeny suggests was already populated by higher‐elevation, congeneric dwarf‐jays (C. argentigula,C. pumilo,C. mirabilis, andC. nanus). The outcome of these events and fortuitous elevational zonation was thatC. cucullatacould continue colonizing new highland areas farther north during the Pleistocene. Resultingly, fourC. cucullatalineages became isolated in allopatric, highland regions from Panama to Mexico, diverging in genetics, morphology, plumage, and vocalizations. At least two of these lineages are best described as species (C. mitrataandC. cucullata). Continued study will further document the influence of the GABI and help clarify how dispersal and vicariance shaped modern‐day species assemblages in the Americas.

     
    more » « less