Molecular signatures of selection associated with host-plant differences in <i>Pieris</i> butterflies

Okamura, Yu; Sato, Ai; Tsuzuki, Natsumi; Murakami, Masashi; Heidel‐Fischer, Hanna M.; Vogel, Heiko

doi:10.1101/627182

Cited by 4 publications

(5 citation statements)

References 39 publications

(8 reference statements)

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“…Recent experiments have shown dramatic regulatory changes in detoxification pathways following host shifts in plant‐feeding arthropods (Dermauw et al., 2013; Govind et al., 2010; Müller et al., 2017; Yu et al., 2016; Zhang et al., 2017). Additionally, other comparative genomic studies have found similar evidence of positive selection in detoxification genes related to host plant utilization (Simon et al., 2015; Gloss et al, 2019; Okamura et al., 2019). Although the proportion of detoxification proteins under selection from the branch‐site test is high in CPB, these values are relatively low in L. tumamoca and L. peninsularis .…”

Section: Discussionmentioning

confidence: 67%

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

et al. 2020

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Contextualizing evolutionary history and identifying genomic features of an insect that might contribute to its pest status is important in developing early detection and control tactics. In order to understand the evolution of pestiferousness, which we define as the accumulation of traits that contribute to an insect population's success in an agroecosystem, we tested the importance of known genomic properties associated with rapid adaptation in the Colorado potato beetle (CPB), Leptinotarsa decemlineata Say. Within the leaf beetle genus Leptinotarsa, only CPB, and a few populations therein, has risen to pest status on cultivated nightshades, Solanum. Using whole genomes from ten closely related Leptinotarsa species native to the United States, we reconstructed a high-quality species tree and used this phylogenetic framework to assess evolutionary patterns in four genomic features of rapid adaptation: standing genetic variation, gene family expansion and contraction, transposable element abundance and location, and positive selection at protein-coding genes. Throughout approximately 20 million years of history, Leptinotarsa species show little evidence of gene family turnover and transposable element variation. However, there is a clear pattern of CPB experiencing higher rates of positive selection on protein-coding genes. We determine that these rates are associated with greater standing genetic variation due to larger effective population size, which supports the theory that the demographic history contributes to rates of protein evolution. Furthermore, we identify a suite of coding genes under positive selection that are putatively associated with pestiferousness in the Colorado potato beetle lineage. They are involved in the biological processes of xenobiotic detoxification, chemosensation and hormone function.

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Section: Discussionmentioning

confidence: 67%

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

et al. 2020

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“…However, all species had relatively high p N / p S and ω compared with other insect taxa (Heger and Ponting 2007; Rouselle et al. 2016; Okamura et al. 2019; Pinharanda et al.…”

Section: Discussionmentioning

confidence: 89%

Dissecting the Effects of Selection and Mutation on Genetic Diversity in Three Wood White (Leptidea) Butterfly Species

Talla

Soler

Kawakami

et al. 2019

Genome Biology and Evolution

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The relative role of natural selection and genetic drift in evolution is a major topic of debate in evolutionary biology. Most knowledge spring from a small group of organisms and originate from before it was possible to generate genome-wide data on genetic variation. Hence, it is necessary to extend to a larger number of taxonomic groups, descriptive and hypothesis-based research aiming at understanding the proximate and ultimate mechanisms underlying both levels of genetic polymorphism and the efficiency of natural selection. In this study, we used data from 60 whole-genome resequenced individuals of three cryptic butterfly species (Leptidea sp.), together with novel gene annotation information and population recombination data. We characterized the overall prevalence of natural selection and investigated the effects of mutation and linked selection on regional variation in nucleotide diversity. Our analyses showed that genome-wide diversity and rate of adaptive substitutions were comparatively low, whereas nonsynonymous to synonymous polymorphism and substitution levels were comparatively high in Leptidea, suggesting small long-term effective population sizes. Still, negative selection on linked sites (background selection) has resulted in reduced nucleotide diversity in regions with relatively high gene density and low recombination rate. We also found a significant effect of mutation rate variation on levels of polymorphism. Finally, there were considerable population differences in levels of genetic diversity and pervasiveness of selection against slightly deleterious alleles, in line with expectations from differences in estimated effective population sizes.

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“…To assess whether seasonal changes in wing morphology and flight behaviours, we study two polyvoltine butterfly species, Pieris napi (Linnaeus, 1758) and P. rapae (Linnaeus, 1758) (Pieridae: Pierini). These two species are closely-related (Okamura et al, 2019), co-occur in Europe and are ecologically very similar (Tenger-Trolander et al, 2023). They are known to differ in wing size and shape in spring and summer (Fric et al, 2006;Shkurikhin & Oslina, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…While P. napi usually flies in habitats such as forest edges and feeds on biennial and perennial plants, P. rapae explores temporary and degraded habitats with ephemeral plants (Ohsaki & Sato, 1999), including agricultural landscapes (Ryan et al, 2019). Seasonal differences in population dynamics driven by climate have also been reported for P. napi and P. rapae (Okamura et al, 2019;von Schmalensee et al, 2023). While P. rapae is more abundant during summer, P. napi has a higher overwintering survival than P. rapae, resulting in higher abundances during the spring (von Schmalensee et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Flight behaviour diverges more between seasonal forms than between species inPierisbutterflies

Kleckova,

Linke,

Rezende

et al. 2023

Preprint

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In flying animals, wing morphology jointly evolves with flight behaviours. Whether seasonal polymorphism in butterfly wing morphology is linked to divergent flight behaviour is however not known. Here we compared the flight behaviour and the morphology between the spring and the summer forms of two closely related, temperate species,Pieris napiandP. rapae. We first quantify three-dimensional flight behaviour by reconstructing individual flight trajectories using stereoscopic high-speed videography in an experimental cage. We then measure wing size and shape characteristics assumed to influence flight behaviours in butterflies. We show that seasonal, but not interspecific, differences in flight behaviour might be associated with divergent forewing shapes, either elongated or rounded wings. InPierisspring forms, individuals are small and have elongated forewings, which are significantly correlated with low speed and acceleration, but with high flight curvature. LargePierissummer individuals exhibit rounded forewings, which are correlated with high flight speed, turning acceleration, and advance ratio. We interpret such results as potentially adaptive flight behaviours inPieris. Curvy flight trajectories in the spring forms may be a specialised foraging behaviour evolving in response to newly emerging feeding and oviposition resources. In contrast, the summer forms’ high flight speed and flight efficiency may be advantageous for dispersal to new habitats. Further, the recorded higher acceleration capacities of the summer form could have evolved in response to higher predation pressure. Our study provides quantitative evidence of divergent flight behaviours between seasonal forms ofPierisbutterflies correlated with differences in wing morphology. Seasonal flight behaviour could be adaptive, possibly driven by the interaction of various seasonal selection pressures, including resource distribution (nectar and larval food plants), predator and parasitoid pressure, and thermoregulation.

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Molecular signatures of selection associated with host-plant differences in Pieris butterflies

Cited by 4 publications

References 39 publications

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

Dissecting the Effects of Selection and Mutation on Genetic Diversity in Three Wood White (Leptidea) Butterfly Species

Flight behaviour diverges more between seasonal forms than between species inPierisbutterflies

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