1. |
- Liénard, Marjorie A., et al.
(author)
-
The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies
- 2021
-
In: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences. - 0027-8424. ; 118:6
-
Journal article (peer-reviewed)abstract
- Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple Gq opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.
|
|
2. |
- Molleman, Freerk, et al.
(author)
-
Quantifying the effects of species traits on predation risk in nature : A comparative study of butterfly wing damage
- 2020
-
In: Journal of Animal Ecology. - : Wiley. - 0021-8790 .- 1365-2656. ; 89:3, s. 716-729
-
Journal article (peer-reviewed)abstract
- Evading predators is a fundamental aspect of the ecology and evolution of all prey animals. In studying the influence of prey traits on predation risk, previous researchers have shown that crypsis reduces attack rates on resting prey, predation risk increases with increased prey activity, and rapid locomotion reduces attack rates and increases chances of surviving predator attacks. However, evidence for these conclusions is nearly always based on observations of selected species under artificial conditions. In nature, it remains unclear how defensive traits such as crypsis, activity levels and speed influence realized predation risk across species in a community. Whereas direct observations of predator–prey interactions in nature are rare, insight can be gained by quantifying bodily damage caused by failed predator attacks. We quantified how butterfly species traits affect predation risk in nature by determining how defensive traits correlate with wing damage caused by failed predation attempts, thereby providing the first robust multi-species comparative analysis of predator-induced bodily damage in wild animals. For 34 species of fruit-feeding butterflies in an African forest, we recorded wing damage and quantified crypsis, activity levels and flight speed. We then tested for correlations between damage parameters and species traits using comparative methods that account for measurement error. We detected considerable differences in the extent, location and symmetry of wing surface loss among species, with smaller differences between sexes. We found that males (but not females) of species that flew faster had substantially less wing surface loss. However, we found no correlation between cryptic coloration and symmetrical wing surface loss across species. In species in which males appeared to be more active than females, males had a lower proportion of symmetrical wing surface loss than females. Our results provide evidence that activity greatly influences the probability of attacks and that flying rapidly is effective for escaping pursuing predators in the wild, but we did not find evidence that cryptic species are less likely to be attacked while at rest.
|
|
3. |
- Valencia-Montoya, Wendy A., et al.
(author)
-
Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)
- 2021
-
In: Proceedings of the Royal Society B: Biological Sciences. - : The Royal Society. - 1471-2954 .- 0962-8452. ; 288:1950
-
Journal article (peer-reviewed)abstract
- Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa. In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage.
|
|