Linkage mapping and genome annotation give novel insights into gene family expansions and regional recombination rate variation in the painted lady (Vanessa cardui) butterfly

Characterization of gene family expansions and crossing over is crucial for understanding how organisms adapt to the environment. Here, we develop a high-density linkage map and detailed genome annotation of the painted lady butterfly (Vanessa cardui) - a non-diapausing, highly polyphagous species famous for its long-distance migratory behavior and almost cosmopolitan distribution. Our results reveal a complex interplay between regional recombination rate variation, gene duplications and transposable element activity shaping the genome structure of the painted lady. We identify several lineage specific gene family expansions. Their functions are mainly associated with protein and fat metabolism, detoxification, and defense against infection - critical processes for the painted lady's unique life-history. Furthermore, the detailed recombination maps allow us to characterize the regional recombination landscape, data that reveal a strong effect of chromosome size on the recombination rate, a limited impact of GC-biased gene conversion and a positive association between recombination and short interspersed elements.

Financial support for this project was provided by FORMAS (Research grant 2019-00670 to N.B.) and The Swedish Collegium for Advanced Science (Natural Sciences Programme, Knut and Alice Wallenberg Foundation, Postdoc funding for D.S.). R.V. was supported by the grant PID2019-107078GB-I00 funded by MCIN/AEI/10.13039/501100011033. G.T. was supported by the grant PID2020-117739GA-I00 funded by MCIN/AEI/10.13039/501100011033 and by “La Caixa” Foundation (ID 100010434) through the grant LCF/BQ/PR19/11700004.

1. Introduction 2. Results 2.1. Linkage map and genome annotation 2.2. Synteny 2.3. Gene family evolution 2.4. Patterns of recombination rate variation 2.4.1. Global and chromosome specific recombination rates 2.4.2. Intra-chromosomal variation in recombination rate and associations with genomic elements 3. Discussion 3.1. The genome of the painted lady butterfly 3.2. Sex chromosomes 3.3. Gene family analysis 3.4. Patterns of recombination rate variation 4. Conclusions 5. Methods 5.1. Linkage map 5.1.1. Sampling and DNA-extraction 5.1.2. Building the linkage map 5.2. Genome annotation and whole genome statistics 5.2.1. Genome assembly statistics 5.2.2. Gene and repeat annotation 5.3. Manual curation 5.4. Gene family evolution 5.5. Gene ontology enrichment 5.6. Recombination rate analysis 5.6.1. Chromosome level analysis 5.6.2. Window-based analysis Data access CRediT authorship contribution statement Declaration of Competing Interest Acknowledgements Appendix A. Supplementary data Data availability References