The impact of biological invasion and genomic local adaptation on the geographical distribution of Aedes aegypti in Panama

Local adaptation is an important consideration when predicting arthropod-borne disease risk because it can impact on vector population fitness and persistence. However, the extent that vector populations are adapted to local environmental conditions and whether this can impact on species distributions generally remains unknown. Here we find that the geographic distribution of Ae. aegypti across Panama is rapidly changing as a consequence of the recent invasion by its ecological competitor, Aedes albopictus. Although Ae. albopictus has displaced Ae. aegypti in some areas, species coexist across many areas, raising the question: What biological and environmental factors permit population persistence?. Despite low population structure and high gene flow in Ae. aegypti across Panama, excepting the province of Bocas del Toro, we identify 128 candidate SNPs, clustered within 17 genes, which show a strong genetic signal of local adaptation. This putatively adaptive variation occurs across relatively fine geographic scales with the composition and frequency of candidate adaptive loci differing between populations in wet tropical environments along the Caribbean coast and the dry tropical conditions typical of the Pacific coast of Panama. Temperature and vegetation were important predictors of adaptive genomic variation in Ae. aegypti with potential areas of local adaptation occurring within the Caribbean region of Bocas del Toro, the Pacific coastal areas of Herrera and Panama City and the eastern Azuero Peninsula. Interestingly, several of these locations coincide with areas where Ae. aegypti and Ae. albopictus co-exist, suggesting that Ae. aegypti could have an adaptive edge under local environmental conditions that impacts on inter-specific competition with Ae. albopictus. Our results guide future experimental work by suggesting that locally adapted Ae. aegypti are able to persist on invasion by Ae. albopictus and, as a consequence, may fundamentally alter future arborviral disease risk and efforts to control mosquito populations.Local adaptation is an important consideration when predicting arthropod-borne disease risk because it can impact on vector population fitness and persistence. However, the extent that vector populations are adapted to local environmental conditions and whether this can impact on species distributions generally remains unknown. Here we find that the geographic distribution of Ae. aegypti across Panama is rapidly changing as a consequence of the recent invasion by its ecological competitor, Aedes albopictus. Although Ae. albopictus has displaced Ae. aegypti in some areas, species coexist across many areas, raising the question: What biological and environmental factors permit population persistence?. Despite low population structure and high gene flow in Ae. aegypti across Panama, excepting the province of Bocas del Toro, we identify 128 candidate SNPs, clustered within 17 genes, which show a strong genetic signal of local adaptation. This putatively adaptive variation occurs across relatively fine geographic scales with the composition and frequency of candidate adaptive loci differing between populations in wet tropical environments along the Caribbean coast and the dry tropical conditions typical of the Pacific coast of Panama. Temperature and vegetation were important predictors of adaptive genomic variation in Ae. aegypti with potential areas of local adaptation occurring within the Caribbean region of Bocas del Toro, the Pacific coastal areas of Herrera and Panama City and the eastern Azuero Peninsula. Interestingly, several of these locations coincide with areas where Ae. aegypti and Ae. albopictus co-exist, suggesting that Ae. aegypti could have an adaptive edge under local environmental conditions that impacts on inter-specific competition with Ae. albopictus. Our results guide future experimental work by suggesting that locally adapted Ae. aegypti are able to persist on invasion by Ae. albopictus and, as a consequence, may fundamentally alter future arborviral disease risk and efforts to control mosquito populations

Convocation

The origins of phenotypic variation within mimetic Heliconius butterflies have long fascinated biologists and naturalists. However, the evolutionary processes that have generated this extraordinary diversity remain puzzling. Here we examine intraspecific variation across Heliconius cydno diversification and compare this variation to that within the closely related H. melpomene and H. timareta radiations. Our data, which consist of both mtDNA and genome scan from nearly 2250 AFLP loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that likely diverged from H. melpomene during the Pliocene-Pleistocene boundary. MtDNA suggest that this radiation originated in Central America or the Northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome-scan data indicate significant admixture among sympatric H. cydno/H.timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno color pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms

Mitogenomic divergence between three pairs of putative geminate fishes from Panama

© 2018, © 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. We sequenced the complete mitochondrial genomes of three pairs of congeneric peripheral fishes distributed on either side of the Isthmus of Panama in order to test their status as geminate species pairs. Our phylogenetic analysis did not support a sister relationship between Gobiomorus dormitor and G. maculatus and therefore they cannot be considered geminates. The average genetic distance of protein-coding genes between Sicydium altum and S. salvini was more than two times larger than between Atlantic and Pacific Awaous banana, suggesting different timings for their divergence across the Isthmus of Panama

Complete mitochondrial genomes of three Neotropical sleeper gobies: Eleotris amblyopsis, E. picta and Hemieleotris latifasciata (Gobiiformes: Eleotridae)

© 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. We report the first complete mitochondrial genomes of three species of eleotrid fishes from the Pacific and Atlantic watersheds of Panama: Eleotris amblyopsis, E. picta, and Hemieleotris latifasciata. The three species have similar mitochondrial genomes with identical gene order; however, there are differences in the length of control region, 16S rRNA, and in seven of the tRNAs. In addition, ATP8 is one codon shorter in E. picta than in E. amblyopsis or H. latifasciata. We infer a phylogeny for Gobiiformes based on all mitochondrial protein-coding genes, which supports the monophyly of Eleotridae but does not recover Neotropical members of Eleotris as a distinct clade

Conservation and flexibility in the gene regulatory landscape of heliconiine butterfly wings

Funder: Wellcome Trust; doi: http://dx.doi.org/10.13039/100004440Abstract: Background: Many traits evolve by cis-regulatory modification, by which changes to noncoding sequences affect the binding affinity for available transcription factors and thus modify the expression profile of genes. Multiple examples of cis-regulatory evolution have been described at pattern switch genes responsible for butterfly wing pattern polymorphism, including in the diverse neotropical genus Heliconius, but the identities of the factors that can regulate these switch genes have not been identified. Results: We investigated the spatial transcriptomic landscape across the wings of three closely related butterfly species, two of which have a convergently evolved co-mimetic pattern and the other having a divergent pattern. We identified candidate factors for regulating the expression of wing patterning genes, including transcription factors with a conserved expression profile in all three species, and others, including both transcription factors and Wnt pathway genes, with markedly different profiles in each of the three species. We verified the conserved expression profile of the transcription factor homothorax by immunofluorescence and showed that its expression profile strongly correlates with that of the selector gene optix in butterflies with the Amazonian forewing pattern element ‘dennis.’ Conclusion: Here we show that, in addition to factors with conserved expression profiles like homothorax, there are also a variety of transcription factors and signaling pathway components that appear to vary in their expression profiles between closely related butterfly species, highlighting the importance of genome-wide regulatory evolution between species

Heliconiini butterflies can learn time-dependent reward associations.

For many pollinators, flowers provide predictable temporal schedules of resource availability, meaning an ability to learn time-dependent information could be widely beneficial. However, this ability has only been demonstrated in a handful of species. Observations of Heliconius butterflies suggest that they may have an ability to form time-dependent foraging preferences. Heliconius are unique among butterflies in actively collecting pollen, a dietary behaviour linked to spatio-temporally faithful 'trap-line' foraging. Time dependency of foraging preferences is hypothesized to allow Heliconius to exploit temporal predictability in alternative pollen resources. Here, we provide the first experimental evidence in support of this hypothesis, demonstrating that Heliconius hecale can learn opposing colour preferences in two time periods. This shift in preference is robust to the order of presentation, suggesting that preference is tied to the time of day and not due to ordinal or interval learning. However, this ability is not limited to Heliconius, as previously hypothesized, but also present in a related genus of non-pollen feeding butterflies. This demonstrates time learning likely pre-dates the origin of pollen feeding and may be prevalent across butterflies with less specialized foraging behaviours

The appearance of mimetic Heliconius butterflies to predators and conspecifics.

Adaptive coloration is under conflicting selection pressures: choosing potential mates and warning signaling against visually guided predators. Different elements of the color signal may therefore be tuned by evolution for different functions. We investigated how mimicry in four pairs of Heliconius comimics is potentially seen both from the perspective of butterflies and birds. Visual sensitivities of eight candidate avian predators were predicted through genetic analysis of their opsin genes. Using digital image color analysis, combined with bird and butterfly visual system models, we explored how predators and conspecifics may visualize mimetic patterns. Ultraviolet vision (UVS) birds are able to discriminate between the yellow and white colors of comimics better than violet vision (VS) birds. For Heliconius vision, males and females differ in their ability to discriminate comimics. Female vision and red filtering pigments have a significant effect on the perception of the yellow forewing band and the red ventral forewing pattern. A behavioral experiment showed that UV cues are used in mating behavior; removal of such cues was associated with an increased tendency to approach comimics as compared to conspecifics. We have therefore shown that visual signals can act to both reduce the cost of confusion in courtship and maintain the advantages of mimicry.ERC, CAPES, STR

Polyphyly and gene flow between non-sibling Heliconius species

BACKGROUND: The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America. RESULTS: In these taxa, we sequenced 30–45 haplotypes per locus of a mitochondrial region containing the genes for cytochrome oxidase subunits I and II (CoI/CoII), and intron-spanning fragments of three unlinked nuclear loci: triose-phosphate isomerase (Tpi), mannose-6-phosphate isomerase (Mpi) and cubitus interruptus (Ci) genes. A fifth gene, dopa decarboxylase (Ddc) produced sequence data likely to be from different duplicate loci in some of the taxa, and so was excluded. Mitochondrial and Tpi genealogies are consistent with reciprocal monophyly, whereas sympatric populations of the species in Panama share identical or similar Mpi and Ci haplotypes, giving rise to genealogical polyphyly at the species level despite evidence for rapid sequence divergence at these genes between geographic races of H. melpomene. CONCLUSION: Recent transfer of Mpi haplotypes between species is strongly supported, but there is no evidence for introgression at the other three loci. Our results demonstrate that the boundaries between animal species can remain selectively porous to gene flow long after speciation, and that introgression, even between non-sibling species, can be an important factor in animal evolution. Interspecific gene flow is demonstrated here for the first time in Heliconius and may provide a route for the transfer of switch-gene adaptations for Müllerian mimicry. The results also forcefully demonstrate how reliance on a single locus may give an erroneous picture of the overall genealogical history of speciation and gene flow

Phenotypic plasticity in chemical defence of butterflies allows usage of diverse host plants.

Host plant specialization is a major force driving ecological niche partitioning and diversification in insect herbivores. The cyanogenic defences of Passiflora plants keep most herbivores at bay, but not the larvae of Heliconius butterflies, which can both sequester and biosynthesize cyanogenic compounds. Here, we demonstrate that both Heliconius cydno chioneus and H. melpomene rosina have remarkable plasticity in their chemical defences. When feeding on Passiflora species with cyanogenic compounds that they can readily sequester, both species downregulate the biosynthesis of these compounds. By contrast, when fed on Passiflora plants that do not contain cyanogenic glucosides that can be sequestered, both species increase biosynthesis. This biochemical plasticity comes at a fitness cost for the more specialist H. m. rosina, as adult size and weight for this species negatively correlate with biosynthesis levels, but not for the more generalist H. c. chioneus. By contrast, H. m rosina has increased performance when sequestration is possible on its specialized host plant. In summary, phenotypic plasticity in biochemical responses to different host plants offers these butterflies the ability to widen their range of potential hosts within the Passiflora genus, while maintaining their chemical defences.UKRI, BBSRC: BB/R007500/1 Horizon 2020 - Marie Curie Actions, grant number: 841230 (Acronym: CyanideEvolution) European Research Council, grant number: 339873 (Acronym: SpeciationGenetics) Danmarks Frie Forskningsfond - FNU: 1323-0008