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Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants.

ABSTRACT: The mega-diversity of herbivorous insects is attributed to their co-evolutionary associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a valuable opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide adaptations and macroevolutionary consequences, lending support to the importance of ecological interactions as evolutionary drivers over long time periods.

SUBMITTER: Allio R

PROVIDER: S-EPMC7806994 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants.

Allio Rémi R Nabholz Benoit B Wanke Stefan S Chomicki Guillaume G Pérez-Escobar Oscar A OA Cotton Adam M AM Clamens Anne-Laure AL Kergoat Gaël J GJ Sperling Felix A H FAH Condamine Fabien L FL

Nature communications 20210113 1

The mega-diversity of herbivorous insects is attributed to their co-evolutionary associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shif ...[more]

PMID: 33441560

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Project description:We illustrate an evolutionary host shift driven by increased fitness on a novel host, despite maladaptation to it in six separate host-adaptive traits. Here, local adaptation is defined as possession of traits that provide advantage in specific environmental contexts; thus individuals can have higher fitness in benign environments to which they are maladapted than in demanding environments to which they are well adapted. A population of the butterfly Euphydryas editha adapted to a long-lived, chemically well-defended host, Pedicularis, had traditionally been under natural selection to avoid the ephemeral, less-defended Collinsia. The lifespan of Collinsia was so short that it senesced before larvae entered diapause. After logging killed Pedicularis in clear-cut patches and controlled burning simultaneously extended Collinsia lifespan, insect fitness on Collinsia in clearings suddenly became higher than on Pedicularis in adjacent unlogged patches. Collinsia was rapidly colonized and preference for it evolved, but insects feeding on it retained adaptations to Pedicularis in alighting bias, two aspects of postalighting oviposition preference, dispersal bias, geotaxis, and clutch size, all acting as maladaptations to Collinsia. Nonetheless, populations boomed on Collinsia in clearings, creating sources that fed pseudosinks in unlogged patches where Pedicularis was still used. After c. 20 years, butterfly populations in clearings disappeared and the metapopulation reverted to Pedicularis-feeding. Here we show, via experimental manipulation of oviposition by local Pedicularis-adapted and imported Collinsia-adapted butterflies, that the highest survival at that time would have been from eggs laid in clearings by butterflies adapted to Collinsia. Second highest were locals on Pedicularis. In third place would have been locals on Collinsia in clearings, because local females maladaptively preferred senescent plants. Collinsia had been colonized despite maladaptation and, after successional changes, abandoned because of it. However, the abandoned Collinsia could still have provided the highest fitness, given appropriate adaptation. The butterflies had tumbled down an adaptive peak.

Project description:BACKGROUND:A molecular population genetics understanding is central to the study of ecological and evolutionary functional genomics. Population genetics identifies genetic variation and its distribution within and among populations, it reveals the demographic history of the populations studied, and can provide indirect insights into historical selection dynamics. Here we use this approach to examine the demographic and selective dynamics acting of a candidate gene involved in plant-insect interactions. Previous work documents the macroevolutionary and historical ecological importance of the nitrile-specifier protein (Nsp), which facilitated the host shift of Pieridae butterflies onto Brassicales host plants approximately 80 Myr ago. RESULTS:Here we assess the microevolutionary dynamics of the Nsp gene by studying the within and among-population variation at Nsp and reference genes in the butterfly Pieris rapae (Small Cabbage White). Nsp exhibits unexpectedly high amounts of amino acid polymorphism, unequally distributed across the gene. The vast majority of genetic variation exists within populations, with little to no genetic differentiation among four populations on two continents. A comparison of synonymous and nonsynonymous substitutions in 70 randomly chosen genes among P. rapae and its close relative Pieris brassicae (Large Cabbage White) finds Nsp to have a significantly relaxed functional constraint compared to housekeeping genes. We find strong evidence for a recent population expansion and no role for strong purifying or directional selection upon the Nsp gene. CONCLUSIONS:The microevolutionary dynamics of the Nsp gene in P. rapae are dominated by recent population expansion and variation in functional constraint across the repeated domains of the Nsp gene. While the high amounts of amino acid diversity suggest there may be significant functional differences among allelic variants segregating within populations, indirect tests of selection could not conclusively identify a signature of historical selection. The importance of using this information for planning future studies of potential performance and fitness consequences of the observed variation is discussed.

Dataset Information

Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants.

Publications

Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants.

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