Large-scale genome-wide study reveals climate adaptive variability in a cosmopolitan pest

Understanding the genetic basis of climatic adaptation is essential for predicting species’ responses to climate change. However, intraspecific variation of these responses arising from local adaptation remains ambiguous for most species. Here, we analyze genomic data from diamondback moth (Plutella xylostella) collected from 75 sites spanning six continents to reveal that climate-associated adaptive variation exhibits a roughly latitudinal pattern. By developing an eco-genetic index that combines genetic variation and physiological responses, we predict that most P. xylostella populations have high tolerance to projected future climates. Using genome editing, a key gene, PxCad, emerged from our analysis as functionally temperature responsive. Our results demonstrate that P. xylostella is largely capable of tolerating future climates in most of the world and will remain a global pest beyond 2050. This work improves our understanding of adaptive variation along environmental gradients, and advances pest forecasting by highlighting the genetic basis for local climate adaptation.


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Life sciences Behavioural & social sciences Ecological, evolutionary & environmental sciences
For a reference copy of the document with all sections, see nature.com/documents/nr-reporting-summary-flat.pdf Ecological, evolutionary & environmental sciences study design All studies must disclose on these points even when the disclosure is negative. For this study, without aiming to identify the differences between gender and age (developmental stages) in responding to climate change, Diamondback moths, Plutella xylostella (Lepidoptera: Plutellidae), regardless of age and sex, were collected from cruciferous vegetable fields in each sampling locations without any manipulations. Field-collected samples were morphologically inspected and genetically checked with COI sequences to confirm their identity. The samples were preserved in 95% alcohol at -80℃ prior to DNA extraction. Samples used in this study represent local populations of the 75 collection sites.
Based on whole genome resequencing studies, especially on insect species, published previously, we followed their rules for sample size determination, i.e. five (fully sequenced) individuals per site should be good enough to give a robust 'picture' of the intrapopulation genomic variability as well as to compare and contrast with individual from other sites. The number of sites was set to give comprehensive coverage of all geographical regions in which this species is present, i.e. we tried our best to collect specimens as many as possible, given the availability of manpower and financial support. Oceania. For such a random sampling scheme, we only sampled once from each site. Our collection covered an extensive scope of the eco-climatic index and areas that support differing numbers of annual generations, including those regions with year-round persistence of DBM to others that are only seasonably suitable for growth and development of the species. In the present study, however, to investigate the adaptive genetic variation associated with contemporary climates, we used a subset of samples from regions in which DBM is able to persist year-round with a positive ecoclimatic index (EI > 0, where populations are subject to seasonally uninterrupted local selection by climatic factors. Before data analysis, we decided to remove the SNPs with a minor allele frequency (MAF) < 5% to generate common SNPs across the genome, based on the criteria applied in comparable studies. In addition, missing rate was high in sequencing data. We thus excluded the SNPs with a missing rate > 10% to retain majority of individuals and SNPs for further analysis, with the aim of reflecting a relatively complete picture of genomic variation.
An average of approximately five individuals from each of the sampling locations were used for DNA extraction and sequencing, making a total of 372 individuals (with adequate quality data) in 78 locations worldwide. All attempts at replication in sampling, sequencing, gene expression analysis of PxCad, CRISPR/Cas9-based genome editing, bioassay (behavioral responses to different temperatures) were successful. We believe that our findings are convincing and reproducible.
Our sampling locations were randomly selected in different regions according to the geographical and climatic conditions that are suitable for growth and development of DBM. Within each location, larvae, pupae and adults were randomly collected from cruciferous vegetable fields. In gene expression analysis of PxCad, a group of thirty vials (15 vials with DBM females and 15 with males) was frozen in liquid nitrogen and used as control, and other groups of vials were exposed to each of the nine distinct temperature treatments. After each of the treatments, moths were immediately frozen in liquid nitrogen. Each group of vials was divided into three replicates: both 15 vials with females and 15 with males were evenly put into three 1.5 ml tubes, respectively. In each replicates, the allocation was random. In CRISPR/Cas9-based genome editing experiment, the fresh eggs from the DBM strain G88, laid within 15 -20 min, were injected. The DBM G88 individuals for laying eggs were chosen randomly. In the Bioassay: behavioral responses to different temperatures, twenty vials with females and twenty with males were then put into a plastic container. Four plastic containers with DBM adults were placed into a climate incubator where DBM adults were exposed to heat shock treatments. The allocation of female and male individuals to plastic containers was random, so was the allocation of plastic containers with DBM individuals to climate incubator.