Genomes of skipper butterflies reveal extensive convergence of wing patterns

Li, Wenlin; Cong, Qian; Shen, Jinhui; Zhang, Jing; Hallwachs, Winnie; Janzen, Daniel H.

doi:10.1073/pnas.1821304116

Cited by 83 publications

(127 citation statements)

References 21 publications

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“…There have been some reports of nuclear microsatellite loci failing to amplify from older museum material (Watts et al ., ; Saarinen & Daniels, ), especially those loci with long allele amplicons (Strange et al ., ; Ugelvig et al ., ). Yet other studies have been very successful in recovering microsatellite markers (Harper et al ., ; Habel et al ., ) or next‐generation sequence data (Heintzman et al ., ; Tin et al ., ; Prosser et al ., ; Sproul & Maddison, ; Li et al ., ) from 19th‐century material. This suggests to us that the difficulty of successfully obtaining nuclear genotypes from historical insect specimens is probably a surmountable methodological challenge, rather than a fundamental feature of this kind of material.…”

Section: Discussionmentioning

confidence: 99%

How old can we go? Evaluating the age limit for effective DNA recovery from historical insect specimens

Lalonde

Marcus

2019

Systematic Entomology

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Historical museum specimens are valuable for exploring population genetics and evolutionary questions because they can provide snapshots of morphological and genetic characteristics from populations over space and time. Unfortunately, DNA found in older museum specimens is frequently degraded, so obtaining genotypes from many individual samples necessary for rigorous molecular population genetic studies is challenging. Previous studies have varied greatly in their success at obtaining genotypes from older preserved insect material. Many well-intentioned collection curators have used research results showing poor preservation of DNA preserved in museum specimens to inform curatorial best practices, in some cases choosing not to allow DNA extraction by destructive sampling because, in their estimation, the likelihood of success would be low. Recent methodological advances in DNA extraction, amplification, and genotyping have allowed some researchers to include mid-19th century samples in molecular genetic analyses. Here we present a robust, high-throughput, and low-cost DNA extraction and genotyping protocol for historical insect specimens employing restriction digests of PCR products followed by high sensitivity electrophoresis. Using this technique, we obtained mitochondrial haplotypes for 100% of 48 New World Junonia butterfly specimens (Nymphalidae) ranging in age from pre-1813 to 1909 and show that the haplotype frequencies obtained are statistically indistinguishable from 20th-century and contemporary reference populations of Junonia (1632 specimens) matched by geographic region. As most extant insect specimens were collected after 1813, based on our findings we would expect that many or even most pinned specimens preserved in museum collections contain usable DNA for mitochondrial haplotyping.

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Section: Discussionmentioning

confidence: 99%

How old can we go? Evaluating the age limit for effective DNA recovery from historical insect specimens

Lalonde

Marcus

2019

Systematic Entomology

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“…See Table S1 for complete specimen data. A piece of thoracic tissue from fresh specimens, and either the abdomen or a leg from pinned museum specimens were used for DNA extraction and genomic library preparation according to our protocols developed previously [21][22][23][24] . We used mate-pair libraries to assemble a reference genome of Hesperia colorado from a single wild-collected specimen, also accompanied by RNAseq for gene annotation.…”

Section: Methodsmentioning

confidence: 99%

Genomics reveals the origins of ancient specimens

Cong¹,

Shen

Zhang

et al. 2019

Preprint

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Centuries of zoological studies amassed billions of specimens in collections worldwide. Genomics of these specimens promises to rejuvenate biodiversity research. The obstacles stem from DNA degradation with specimen age. Overcoming this challenge, we set out to resolve a series of longstanding controversies involving a group of butterflies. We deduced geographical origins of several ancient specimens of uncertain provenance that are at the heart of these debates. Here, genomics tackles one of the greatest problems in zoology: countless old, poorly documented specimens that serve as irreplaceable embodiments of species concepts. The ability to figure out where they were collected will resolve many on-going disputes. More broadly, we show the utility of genomics applied to ancient museum specimens to delineate the boundaries of species and populations, and to hypothesize about genotypic determinants of phenotypic traits.A study of an animal starts from its name, which is governed by strict rules 1 . A specimen termed the namebearing type represents a species 1 . The lectotype specimen 1 of Homo sapiens is Carl Linnaeus, the father of taxonomy 2 . Populations conspecific with the type carry its name. If two types are conspecific, the earlier name is used. Because most animals were named over a century ago, their types are old and lack details about their collection localities. Historically, phenotypic similarity to the type and its geographic locality determined conspecificity. For cryptic species and uncertain type localities, the phenotypic approach is problematic, leading to heated debates 3-7 . We devised a strategy to obtain genomic sequences of old type specimens and determine to which present-day populations they correspond. To solve a daunting biological problem, we applied this strategy to the skipper butterfly Hesperia comma and its relatives. It is the most important skipper, because the whole family of butterflies (Hesperiidae, the skippers) is typified by the genus Hesperia, and the type of that genus is H. comma, as designated by Carl Linnaeus himself. Several mysteries surround these butterflies. (1) Like the Linnaean type of comma, the type of its American counterpart, Hesperia colorado, collected by noted naturalist Theodore Mead 3,4 , lacks a locality label. Where was this type collected? The answer will seal the fate of names later given to populations of this species. (2) Are American comma-like butterflies the same species as comma in Europe? (3) Unusually for butterflies, Hesperia inhabits a wide range of elevations, from lowlands to alpine zone at over 3500 m. What are the genetic determinants of this elevational plasticity? Genomic data provide clear answers to all these questions.

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“…Therefore, we replaced the clades for each family in these trees with the trees constructed for each individual butterfly family using python ETE3 module (109) to generate the USC butterfly trees used in this study. These trees were rescaled as previously described (39,110) and the time axis was added to the tree constructed from all nuclear genes based on our published calibration (8) to match the ages of common nodes between the current and previous trees.…”

Section: Phylogenetic Analysis Of Usc Butterfliesmentioning

confidence: 99%

Genomics of a complete butterfly continent

Zhang

Cong

Shen

et al. 2019

Preprint

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Never before have we had the luxury of choosing a continent, picking a large phylogenetic group of animals, and obtaining genomic data for its every species. Here, we sequence all 845 species of butterflies recorded from North America north of Mexico. Our comprehensive approach reveals the pattern of diversification and adaptation occurring in this phylogenetic lineage as it has spread over the continent, which cannot be seen on a sample of selected species. We observe bursts of diversification that generated taxonomic ranks: subfamily, tribe, subtribe, genus, and species. The older burst around 70 Mya resulted in the butterfly subfamilies, with the major evolutionary inventions being unique phenotypic traits shaped by high positive selection and gene duplications. The recent burst around 5 Mya is caused by explosive radiation in diverse butterfly groups associated with diversification in transcription and mRNA regulation, morphogenesis, and mate selection. Rapid radiation correlates with more frequent introgression of speciation-promoting and beneficial genes among radiating species. Radiation and extinction patterns over the last 100 million years suggest the following general model of animal evolution. A population spreads over the land, adapts to various conditions through mutations, and diversifies into several species. Occasional hybridization between these species results in accumulation of beneficial alleles in one, which eventually survives, while others become extinct. Not only butterflies, but also the hominids may have followed this path.Butterflies are among the most beloved animals , beautiful and harmless, they have attracted human attention since prehistoric times (1). Being one of the best-studied insects phenotypically (2), butterflies remain largely unexplored by genomics. Until recently, genomic studies of butterflies were confined to a couple of model organisms and pests, such as Heliconius, monarch, and cabbage white, with initial studies leading to groundbreaking insights into mimicry, migration, and toxin resistance (3-5). We have been expanding these efforts on butterfly genomics to cover a broader range of species (6-11). With the rapid decrease in the price of DNA sequencing and the constant development of analytical methods, the time is ripe to sequence the genomes of all butterfly species over a continent.

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Genomes of skipper butterflies reveal extensive convergence of wing patterns

Cited by 83 publications

References 21 publications

How old can we go? Evaluating the age limit for effective DNA recovery from historical insect specimens

How old can we go? Evaluating the age limit for effective DNA recovery from historical insect specimens

Genomics reveals the origins of ancient specimens

Genomics of a complete butterfly continent

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