Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Valencia-Montoya, Wendy A; Elfékih, Samia; North, Henry L.; Meier, Joana I.; Warren, Ian A.; Tay, Wee Tek; Gordon, Karl; Specht, Alexandre; Paula‐Moraes, Silvana V.; Rane, Rahul; Walsh, Tom; Jiggins, Chris D.

doi:10.1093/molbev/msaa108

Cited by 81 publications

(137 citation statements)

References 105 publications

(207 reference statements)

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“…Extensive heterogeneity in the extent of admixture across genomes has been reported in multiple studies of closely related species, including trees (Wang et al., 2020), insects (Martin et al., 2019; Valencia‐Montoya et al., 2020) and cichlid fish (Gante et al., 2016, Svardal et al, 2020). Tracts of the southern O. korogwe genome with extensive evidence for hybridization (e.g., LG7, LG9 and LG17) may have resulted from introgressed alleles in those regions being favoured by selection.…”

Section: Discussionmentioning

confidence: 98%

Newly discovered cichlid fish biodiversity threatened by hybridization with non‐native species

et al. 2020

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Invasive freshwater fishes are known to readily hybridize with indigenous congeneric species, driving loss of unique and irreplaceable genetic resources. Here we reveal that newly discovered (2013–2016) evolutionarily significant populations of Korogwe tilapia (Oreochromis korogwe) from southern Tanzania are threatened by hybridization with the larger invasive Nile tilapia (Oreochromis niloticus). We use a combination of morphology, microsatellite allele frequencies and whole genome sequences to show that O. korogwe from southern lakes (Nambawala, Rutamba and Mitupa) are distinct from geographically disjunct populations in northern Tanzania (Zigi River and Mlingano Dam). We also provide genetic evidence of O. korogwe × niloticus hybrids in three southern lakes and demonstrate heterogeneity in the extent of admixture across the genome. Finally, using the least admixed genomic regions we estimate that the northern and southern O. korogwe populations most plausibly diverged ~140,000 years ago, suggesting that the geographical separation of the northern and southern groups is not a result of a recent translocation, and instead these populations represent independent evolutionarily significant units. We conclude that these newly discovered and phenotypically unique cichlid populations are already threatened by hybridization with an invasive species, and propose that these irreplaceable genetic resources would benefit from conservation interventions.

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Section: Discussionmentioning

confidence: 98%

Newly discovered cichlid fish biodiversity threatened by hybridization with non‐native species

et al. 2020

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“…Indeed, global movements of invasive pests, exemplified by the spread of FAW, as well as the multiple introductions of H. armigera into the South American continent 15 and various Caribbean nations 121 from Asia 10,14 and various Old World regions 3 , are timely reminders of the need for global coordination of enhanced biosecurity preparedness strategies that build on advancement in genomic research. The potential negative impacts of introductions of alien species include introgression of genetic traits to local species through hybridisation 10,13,14,16,28 . Development of new trans-continental trade routes to increase economic growth between trading partners must therefore recognise the significant risks and take into consideration the biosecurity implications associated with the rapid spreading of highly invasive pests and pathogens of plants, animals and humans 122 that could instead undermine the aim to grow the global economy.…”

Section: Discussionmentioning

confidence: 99%

“…This noctuid moth’s wide host range, flight ability 9 and ability to develop resistance to insecticides 10 has enabled establishment across the New World with significant economic 11,12 , and ecological consequences. Importantly, the availability of samples from early stages in the invasion has made it possible to distinguish demographic from adaptive evolutionary processes, as well as to study hybridization upon second contact with a sister species 13–16 .…”

Section: Introductionmentioning

confidence: 99%

Global FAW population genomic signature supports complex introduction events across the Old World

Tay

Rane

Padovan

et al. 2020

Preprint

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Accurate genomic knowledge can elucidate the global spread patterns of invasive pests. The highprofile invasive agricultural pest Spodoptera frugiperda (fall armyworm; FAW) is a case in point. Native to the Americas, the FAW was first reported in West Africa in 2016 and has rapidly spread to over 64 countries across the Old World, resulting in significant economic losses. The chronological order of reported detections has led to the hypothesis that the FAW moved eastwards across Africa and then Asia, however genomic evidence remains lacking to test this hypothesis and to identify the potential origin of invasive populations. Using a whole genome sequencing approach, we explored the population genomic signatures of FAW populations from the Americas and the Old World. Analyses of complete mitochondrial DNA genomes identified 12 maternal lineages across the invasive range, while genomic signatures from 870 high-quality nuclear genome-wide single nucleotide polymorphic (SNP) DNA markers identified five distinct New World populations that broadly reflected their native geographical ranges and absence of host-plant preference status. Unique FAW populations in the Old World were also identified that suggested multiple introductions underpinned their rapid global spread. We identified in Asian FAW individuals, genomes lacking evidence of admixture; while analysis of identified complex substructure revealed significant directional geneflow from Asia into East Africa, in contrast to a simple east-towest spread. Our study highlights the need for population genomics approaches in analysing complex pest invasions, and the importance of international partnership to address global biosecurity challenges presented by emerging high priority insect pests. Correspondence

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“…Our work therefore adds to a growing body of evidence for a profound role of modularity and introgression in the evolution of mimicry in Heliconius butterflies. Furthermore, our results along with examples such as pesticide resistance in mice and Helicoverpa moths (Song et al 2011;Valencia-Montoya et al 2020), beak adaptations in Darwin's finches (Grant and Grant 2010;Lamichhaney et al 2015), vectorial capacity in mosquitoes (Fontaine et al 2015), and human evolution (Abi-Rached et al 2011;Huerta-Sánchez et al 2014;Sankararaman et al 2016) highlight the potential for introgression to act as an adaptive facilitator. There is no identified element for broken band due to a lack of shared ancestry and its independent evolution in each species.…”

Section: Modularity Of Mimicry Facilitates Pattern Switchingmentioning

confidence: 54%

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry

et al. 2020

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Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows colour pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its co-mimics, Heliconius elevatus and Heliconius besckei, around three known major colour patterning genes optix, WntA and cortex. While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant co-mimic Heliconius erato. Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius colour pattern mimicry.

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Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Cited by 81 publications

References 105 publications

Newly discovered cichlid fish biodiversity threatened by hybridization with non‐native species

Newly discovered cichlid fish biodiversity threatened by hybridization with non‐native species

Global FAW population genomic signature supports complex introduction events across the Old World

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry

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