The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera

Ahola, Virpi; Lehtonen, Rainer; Somervuo, Panu; Salmela, Leena; Koskinen, Patrik; Rastas, Pasi; Välimäki, Niko; Paulín, Lars; Kvist, Jouni; Wahlberg, Niklas; Tanskanen, Jaakko; Hornett, Emily A.; Ferguson, Laura; Luo, Shiqi; Cao, Zijuan; Jong, Maaike de; Duplouy, Anne; Smolander, Olli‐Pekka; Vogel, Heiko; McCoy, Rajiv C.; Qian, Keping; Chong, Wong Swee; Zhang, Qin; Ahmad, Freed; Haukka, J; Joshi, Aruj; Salojärvi, Jarkko; Wheat, Christopher W.; Große-Wilde, Ewald; Hughes, Daniel; Katainen, Riku; Pitkänen, Esa; Ylinen, Johannes; Waterhouse, Robert M.; Turunen, Mikko; Vähärautio, Anna; Ojanen, Sami P.; Schulman, Alan H.; Taipale, Minna; Lawson, Daniel; Ukkonen, Esko; Mäkinen, Veli; Goldsmith, Marian R.; Holm, Liisa; Auvinen, Petri; Frilander, Mikko J.; Hanski, Ilkka

doi:10.1038/ncomms5737

Cited by 214 publications

(295 citation statements)

References 69 publications

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“…In the other, six sets of S. litura chromosomes were fused, corresponding to six H. melpomene chromosomes (N = 21) 11 , and another eight S. litura chromosomes were fused, corresponding to four other H. melpomene chromosomes. These changes were consistent with previous reports on chromosome evolution among butterflies including Melitaea cinxia 12 and the moth Manduca sexta 13 …”

Section: Articlessupporting

confidence: 93%

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

et al. 2017

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The tobacco cutworm, Spodoptera litura, is among the most widespread and destructive agricultural pests, feeding on over 100 crops throughout tropical and subtropical Asia. By genome sequencing, physical mapping and transcriptome analysis, we found that the gene families encoding receptors for bitter or toxic substances and detoxification enzymes, such as cytochrome P450, carboxylesterase and glutathione-S-transferase, were massively expanded in this polyphagous species, enabling its extraordinary ability to detect and detoxify many plant secondary compounds. Larval exposure to insecticidal toxins induced expression of detoxification genes, and knockdown of representative genes using short interfering RNA (siRNA) reduced larval survival, consistent with their contribution to the insect’s natural pesticide tolerance. A population genetics study indicated that this species expanded throughout southeast Asia by migrating along a South India–South China–Japan axis, adapting to wide-ranging ecological conditions with diverse host plants and insecticides, surviving and adapting with the aid of its expanded detoxification systems. The findings of this study will enable the development of new pest management strategies for the control of major agricultural pests such as S. litura.

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Section: Articlessupporting

confidence: 93%

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

et al. 2017

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“…hanski@helsinki.fi. populations for 222 SNPs distributed across the genome of the Glanville fritillary (33) to answer these questions. We compare 34 putative neutral SNPs with SNPs from potential candidate genes to identify outliers and hence potential targets for selection.…”

Section: Significancementioning

confidence: 99%

Predictable allele frequency changes due to habitat fragmentation in the Glanville fritillary butterfly

Fountain

Nieminen

Sirén

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Describing the evolutionary dynamics of now extinct populations is challenging, as their genetic composition before extinction is generally unknown. The Glanville fritillary butterfly has a large extant metapopulation in the Åland Islands in Finland, but declined to extinction in the nearby fragmented southwestern (SW) Finnish archipelago in the 20th century. We genotyped museum samples for 222 SNPs across the genome, including SNPs from candidate genes and neutral regions. SW Finnish populations had significantly reduced genetic diversity before extinction, and their allele frequencies gradually diverged from those in contemporary Åland populations over 80 y. We identified 15 outlier loci among candidate SNPs, mostly related to flight, in which allele frequencies have changed more than the neutral expectation. At outlier loci, allele frequencies in SW Finland shifted in the same direction as newly established populations deviated from old local populations in contemporary Åland. Moreover, outlier allele frequencies in SW Finland resemble those in fragmented landscapes as opposed to continuous landscapes in the Baltic region. These results indicate selection for genotypes associated with good colonization capacity in the highly fragmented landscape before the extinction of the populations. Evolutionary response to habitat fragmentation may have enhanced the viability of the populations, but it did not save the species from regional extinction in the face of severe habitat loss and fragmentation. These results highlight a potentially common situation in changing environments: evolutionary changes are not strong enough to fully compensate for the direct adverse effects of environmental change and thereby rescue populations from extinction.

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“…We have shown that, not only is there little evidence for substantial, fixed inversions between H. melpomene and H. cydno , but also that H. melpomene and H. erato , which last shared a common ancestor over 10 million years ago, have largely collinear genomes, and it is also known that there is substantial chromosomal synteny across the Nymphalids (Ahola et al. 2014). The association of multiple inversions with the wing pattern polymorphism in H. numata is all the more remarkable given the low background rate of inversions in these butterflies.…”

Section: Discussionmentioning

confidence: 99%

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

et al. 2017

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Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of coadapted gene combinations. The sympatric butterfly species Heliconius melpomene and Heliconius cydno are separated by many strong barriers, but the species still hybridize infrequently in the wild, and around 40% of the genome is influenced by introgression. We tested the hypothesis that genetic barriers between the species are maintained by inversions or other mechanisms that reduce between‐species recombination rate. We constructed fine‐scale recombination maps for Panamanian populations of both species and their hybrids to directly measure recombination rate within and between species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.

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The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera

Cited by 214 publications

References 69 publications

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

Predictable allele frequency changes due to habitat fragmentation in the Glanville fritillary butterfly

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

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