Cargando…

Migratory behaviour is positively associated with genetic diversity in butterflies

Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost–benefit trade‐offs at the species level. Migratory insects in particular often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic...

Descripción completa

Detalles Bibliográficos
Autores principales: García‐Berro, Aurora, Talla, Venkat, Vila, Roger, Wai, Hong Kar, Shipilina, Daria, Chan, Kok Gan, Pierce, Naomi E., Backström, Niclas, Talavera, Gerard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100375/
https://www.ncbi.nlm.nih.gov/pubmed/36336800
http://dx.doi.org/10.1111/mec.16770
_version_ 1785025264521052160
author García‐Berro, Aurora
Talla, Venkat
Vila, Roger
Wai, Hong Kar
Shipilina, Daria
Chan, Kok Gan
Pierce, Naomi E.
Backström, Niclas
Talavera, Gerard
author_facet García‐Berro, Aurora
Talla, Venkat
Vila, Roger
Wai, Hong Kar
Shipilina, Daria
Chan, Kok Gan
Pierce, Naomi E.
Backström, Niclas
Talavera, Gerard
author_sort García‐Berro, Aurora
collection PubMed
description Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost–benefit trade‐offs at the species level. Migratory insects in particular often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic data to investigate levels of heterozygosity and long‐term population size dynamics in migratory insects, as an alternative to classical local and short‐term approaches such as regional field monitoring. We analyse whole‐genome sequences from 97 Lepidoptera species and show that individuals of migratory species have significantly higher levels of genome‐wide heterozygosity, a proxy for effective population size, than do nonmigratory species. Also, we contribute whole‐genome data for one of the most emblematic insect migratory species, the painted lady butterfly (Vanessa cardui), sampled across its worldwide distributional range. This species exhibits one of the highest levels of genomic heterozygosity described in Lepidoptera (2.95 ± 0.15%). Coalescent modelling (PSMC) shows historical demographic stability in V. cardui, and high effective population size estimates of 2–20 million individuals 10,000 years ago. The study reveals that the high risks associated with migration and local environmental fluctuations do not seem to decrease overall genetic diversity and demographic stability in migratory Lepidoptera. We propose a “compensatory” demographic model for migratory r‐strategist organisms in which local bottlenecks are counterbalanced by reproductive success elsewhere within their typically large distributional ranges. Our findings highlight that the boundaries of populations are substantially different for sedentary and migratory insects, and that, in the latter, local and even regional field monitoring results may not reflect whole population dynamics. Genomic diversity patterns may elucidate key aspects of an insect's migratory nature and population dynamics at large spatiotemporal scales.
format Online
Article
Text
id pubmed-10100375
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-101003752023-04-14 Migratory behaviour is positively associated with genetic diversity in butterflies García‐Berro, Aurora Talla, Venkat Vila, Roger Wai, Hong Kar Shipilina, Daria Chan, Kok Gan Pierce, Naomi E. Backström, Niclas Talavera, Gerard Mol Ecol ORIGINAL ARTICLES Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost–benefit trade‐offs at the species level. Migratory insects in particular often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic data to investigate levels of heterozygosity and long‐term population size dynamics in migratory insects, as an alternative to classical local and short‐term approaches such as regional field monitoring. We analyse whole‐genome sequences from 97 Lepidoptera species and show that individuals of migratory species have significantly higher levels of genome‐wide heterozygosity, a proxy for effective population size, than do nonmigratory species. Also, we contribute whole‐genome data for one of the most emblematic insect migratory species, the painted lady butterfly (Vanessa cardui), sampled across its worldwide distributional range. This species exhibits one of the highest levels of genomic heterozygosity described in Lepidoptera (2.95 ± 0.15%). Coalescent modelling (PSMC) shows historical demographic stability in V. cardui, and high effective population size estimates of 2–20 million individuals 10,000 years ago. The study reveals that the high risks associated with migration and local environmental fluctuations do not seem to decrease overall genetic diversity and demographic stability in migratory Lepidoptera. We propose a “compensatory” demographic model for migratory r‐strategist organisms in which local bottlenecks are counterbalanced by reproductive success elsewhere within their typically large distributional ranges. Our findings highlight that the boundaries of populations are substantially different for sedentary and migratory insects, and that, in the latter, local and even regional field monitoring results may not reflect whole population dynamics. Genomic diversity patterns may elucidate key aspects of an insect's migratory nature and population dynamics at large spatiotemporal scales. John Wiley and Sons Inc. 2022-11-23 2023-02 /pmc/articles/PMC10100375/ /pubmed/36336800 http://dx.doi.org/10.1111/mec.16770 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle ORIGINAL ARTICLES
García‐Berro, Aurora
Talla, Venkat
Vila, Roger
Wai, Hong Kar
Shipilina, Daria
Chan, Kok Gan
Pierce, Naomi E.
Backström, Niclas
Talavera, Gerard
Migratory behaviour is positively associated with genetic diversity in butterflies
title Migratory behaviour is positively associated with genetic diversity in butterflies
title_full Migratory behaviour is positively associated with genetic diversity in butterflies
title_fullStr Migratory behaviour is positively associated with genetic diversity in butterflies
title_full_unstemmed Migratory behaviour is positively associated with genetic diversity in butterflies
title_short Migratory behaviour is positively associated with genetic diversity in butterflies
title_sort migratory behaviour is positively associated with genetic diversity in butterflies
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100375/
https://www.ncbi.nlm.nih.gov/pubmed/36336800
http://dx.doi.org/10.1111/mec.16770
work_keys_str_mv AT garciaberroaurora migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT tallavenkat migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT vilaroger migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT waihongkar migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT shipilinadaria migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT chankokgan migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT piercenaomie migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT backstromniclas migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies
AT talaveragerard migratorybehaviourispositivelyassociatedwithgeneticdiversityinbutterflies