Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings

Understanding how large-scale environmental variability may shape the distribution of phenotypic variation remains central to evolutionary biology. Across-species comparisons of trait variation alongside environmental gradients may offer valuable insights into how different species may respond to si...

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Main Authors: Daniela Polic, Yeşerin Yıldırım, Roger Vila, Paulo Ricardo Ribeiro Cardoso, Markus Franzén, Anders Forsman
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fevo.2023.1087859/full
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author Daniela Polic
Yeşerin Yıldırım
Roger Vila
Paulo Ricardo Ribeiro Cardoso
Markus Franzén
Anders Forsman
author_facet Daniela Polic
Yeşerin Yıldırım
Roger Vila
Paulo Ricardo Ribeiro Cardoso
Markus Franzén
Anders Forsman
author_sort Daniela Polic
collection DOAJ
description Understanding how large-scale environmental variability may shape the distribution of phenotypic variation remains central to evolutionary biology. Across-species comparisons of trait variation alongside environmental gradients may offer valuable insights into how different species may respond to similar selective pressures. We conducted a comparative morphological study (>32° latitude and >47° longitude) on three closely related Argynnini butterfly species, Speyeria aglaja, Fabriciana adippe, and F. niobe. We measured wing size and coloration to assess (1) whether they respond similarly or differently to environmental factors (longitude, latitude, altitude, temperature, precipitation, solar radiation, wind speed); (2) if these factors correspond with those associated with the species’ genetic structure based on a previous study; and (3) whether correlations between phenotypic traits within individuals are species-specific. We found common and species-specific associations of climatic (precipitation, wind speed) and geographic (longitude, altitude) factors with the composite phenotypic variation. Wing size was associated with different variables in the studied species, while melanisation mainly increased in cooler regions in all species, suggesting that the need for temperature regulation is a strong selective pressure on melanisation. Wing size was associated with the genetic structure in all species, highlighting the functional importance of this trait. The environmental drivers associated with the phenotypic variation in S. aglaja and F. adippe were largely the same as those associated with their genetic structure, hinting at a genetic underpinning of the observed morphological variation due to local adaption. We report some distinct intraspecific trait correlations in S. aglaja and F. adippe, indicative of independent phenotypic integration. These phenotypes seem to be associated with protection against predators and thermal regulation in the respective habitats of both species, suggesting that similar selective pressures have resulted in the evolution of different trait combinations. Some of the inter-specific differences could be related to diverging niche breadths and dispersal capacities, exemplifying that the evolution of trait integration and spatial phenotypic differentiation may differ between closely related species with overlapping distribution ranges. Our findings highlight the importance of comparative assessments of variation, and demonstrate that the relative effects of drivers of variability may vary between sister species.
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spelling doaj.art-df4462a66e9244cc900f79a13ec861272023-06-22T11:12:52ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2023-06-011110.3389/fevo.2023.10878591087859Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wingsDaniela Polic0Yeşerin Yıldırım1Roger Vila2Paulo Ricardo Ribeiro Cardoso3Markus Franzén4Anders Forsman5Department of Biology and Environmental Science, Linnaeus University, Kalmar, SwedenDepartment of Biology and Environmental Science, Linnaeus University, Kalmar, SwedenInstitut de Biologia Evolutiva (CSIC), Universitat Pompeu Fabra, Barcelona, SpainInstitut de Biologia Evolutiva (CSIC), Universitat Pompeu Fabra, Barcelona, SpainDepartment of Biology and Environmental Science, Linnaeus University, Kalmar, SwedenDepartment of Biology and Environmental Science, Linnaeus University, Kalmar, SwedenUnderstanding how large-scale environmental variability may shape the distribution of phenotypic variation remains central to evolutionary biology. Across-species comparisons of trait variation alongside environmental gradients may offer valuable insights into how different species may respond to similar selective pressures. We conducted a comparative morphological study (>32° latitude and >47° longitude) on three closely related Argynnini butterfly species, Speyeria aglaja, Fabriciana adippe, and F. niobe. We measured wing size and coloration to assess (1) whether they respond similarly or differently to environmental factors (longitude, latitude, altitude, temperature, precipitation, solar radiation, wind speed); (2) if these factors correspond with those associated with the species’ genetic structure based on a previous study; and (3) whether correlations between phenotypic traits within individuals are species-specific. We found common and species-specific associations of climatic (precipitation, wind speed) and geographic (longitude, altitude) factors with the composite phenotypic variation. Wing size was associated with different variables in the studied species, while melanisation mainly increased in cooler regions in all species, suggesting that the need for temperature regulation is a strong selective pressure on melanisation. Wing size was associated with the genetic structure in all species, highlighting the functional importance of this trait. The environmental drivers associated with the phenotypic variation in S. aglaja and F. adippe were largely the same as those associated with their genetic structure, hinting at a genetic underpinning of the observed morphological variation due to local adaption. We report some distinct intraspecific trait correlations in S. aglaja and F. adippe, indicative of independent phenotypic integration. These phenotypes seem to be associated with protection against predators and thermal regulation in the respective habitats of both species, suggesting that similar selective pressures have resulted in the evolution of different trait combinations. Some of the inter-specific differences could be related to diverging niche breadths and dispersal capacities, exemplifying that the evolution of trait integration and spatial phenotypic differentiation may differ between closely related species with overlapping distribution ranges. Our findings highlight the importance of comparative assessments of variation, and demonstrate that the relative effects of drivers of variability may vary between sister species.https://www.frontiersin.org/articles/10.3389/fevo.2023.1087859/fullevolutiongeographymelanismphenotypic integrationthermal environmentwing coloration
spellingShingle Daniela Polic
Yeşerin Yıldırım
Roger Vila
Paulo Ricardo Ribeiro Cardoso
Markus Franzén
Anders Forsman
Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
Frontiers in Ecology and Evolution
evolution
geography
melanism
phenotypic integration
thermal environment
wing coloration
title Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
title_full Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
title_fullStr Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
title_full_unstemmed Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
title_short Large-scale spatial variation and phenotypic integration in three Argynnini species inform about functions and evolutionary drivers of butterfly wings
title_sort large scale spatial variation and phenotypic integration in three argynnini species inform about functions and evolutionary drivers of butterfly wings
topic evolution
geography
melanism
phenotypic integration
thermal environment
wing coloration
url https://www.frontiersin.org/articles/10.3389/fevo.2023.1087859/full
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