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

Abstract

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.

Genetic structure, UV‐vision, wing coloration and size coincide with colour polymorphism in Fabriciana adippe butterflies

“…A difference in wing size between colour morphs in F. adippe was also apparent in a study based on analyses of phenotypic data collected across a large spatial scale (>32° latitude and >47° longitude), with individuals belonging to the adippe morph having significantly larger wings than cleodoxa (see table S1 in Polic et al. (2023)). Still, firm evaluation of the hypothesis that these colour morphs represent alternative adaptive peaks associated with different microhabitats (i.e.…”

“…To obtain data on body size and wing colour patterns, each butterfly was photographed in front of standard white paper with a Nikon D3000 camera using an 18–55 mm lens without flash, with the left ventral fore‐ and hindwing and the right dorsal fore‐ and hindwing (i.e. four parts) facing the camera, together with a ruler (Polic et al., 2023). The camera was placed in a fixed position, that is, 34 cm from the wings.…”

“…In each of the 4 wing parts (left ventral fore‐ and hindwing, right dorsal fore‐ and hindwing), we used the “select by colour” tool to select and measure the number of pixels of a certain colour, viz. “light brown” (#92580f), “dark brown” (#4a3822), “black” (#0a0907), “light orange” (#c88d00), “dark orange” (#a55400), “white” (#f2f4e7), “grey” (#b5b498), “yellow” (#c5a035), “light green” (#7b7f20), and “dark green” (#565d17) with a threshold of 15 (Polic et al., 2023). Then, we calculated the percentage of each colour in each wing part.…”

“…relative fitness) of individuals, for example, by influencing susceptibility to predators, intraspecific signalling for mate choice, capacity for temperature regulation, protection from UV‐radiation and resistance to desiccation and abrasion (Huey & Kingsolver, 1989; Ruxton et al., 2004; Wellenreuther et al., 2014). Because animal colour patterns have multifarious functions, a change in one component may induce selection that modifies the combination of size, shape, colour and position of other pattern components, and this may contribute to the integration and differentiation of multiple colour pattern elements (Fisher, 1930; Nijhout, 1991; Polic et al., 2023; Tsai et al., 2020). In many species, colour patterns are associated with body size, behaviours or other phenotypic traits (Ahnesjö & Forsman, 2003; Forsman et al., 2008; McKinnon & Pierotti, 2010; True, 2003).…”

“…Polic et al (2023)). Still, firm evaluation of the hypothesis that these colour morphs represent alternative adaptive peaks associated with different microhabitats (i.e.…”