Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms

Castiglione, Gianni M; Schott, Ryan K.; Hauser, Frances E.; Chang, Belinda S. W.

doi:10.1111/evo.13396

Cited by 20 publications

(23 citation statements)

References 97 publications

(444 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…This nicely illustrates that convergent phenotypic evolution occurred via different routes, as also suggested for adaptive evolution of the dim‐light sensitive rhodopsin (Castiglione et al. ). However, at this point, we are still lacking knowledge about the underlying molecular bases for the observed gene expression differences that produced the convergent changes in visual sensitivity.…”

Section: Discussionsupporting

confidence: 71%

“…; Castiglione et al. ) molecular mechanisms. We found that across our study species, varying subsets of cone opsin genes (as well as cyp27c1 ) were differentially expressed among the three environments, that is adjustment of the visual system to new environments occurred by changing expression of single cone opsins, the two green‐sensitive rh2a genes and/or the red‐sensitive lws , as well as cyp27c1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Convergent phenotypic evolution of the visual system via different molecular routes: How Neotropical cichlid fishes adapt to novel light environments

2018

View full text Add to dashboard Cite

How predictable is evolution? This remains a fundamental but contested issue in evolutionary biology. When independent lineages colonize the same environment, we are presented with a natural experiment that allows us to ask if genetic and ecological differences promote species‐specific evolutionary outcomes or whether species phenotypically evolve in a convergent manner in response to shared selection pressures. If so, are the molecular mechanisms underlying phenotypic convergence the same? In Nicaragua, seven species of cichlid fishes concurrently colonized two novel photic environments. Hence, their visual system represents a compelling model to address these questions, particularly since the adaptive value of phenotypic changes is well‐understood. By analyzing retinal transcriptomes, we found that differential expression of genes responsible for color vision (cone opsins and cyp27c1) produced rapid and mostly convergent changes of predicted visual sensitivities. Notably, these changes occurred in the same direction in all species although there were differences in underlying gene expression patterns illustrating nonconvergence at the molecular level. Adaptive phenotypes evolved deterministically, even when species differ substantially in ecology and genetic variation. This provides strong evidence that phenotypic evolution of the visual system occurred in response to similar selective forces of the photic environment.

show abstract

Section: Discussionsupporting

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Convergent phenotypic evolution of the visual system via different molecular routes: How Neotropical cichlid fishes adapt to novel light environments

2018

View full text Add to dashboard Cite

show abstract

“…These models have been increasingly applied to evaluate whether complex ecological aspects (e.g. foraging depth and habitat) and evolutionary transitions may have influenced divergent evolutionary rates in distinct lineages in a wide range of vertebrate groups [32][33][34][35][36][37][38][39]. We predicted that ecological specializations associated with diminished reliance on visual cues (e.g.…”

Section: Introductionmentioning

confidence: 99%

The role of ecological factors in shaping bat cone opsin evolution

et al. 2018

Self Cite

View full text Add to dashboard Cite

Bats represent one of the largest and most striking nocturnal mammalian radiations, exhibiting many visual system specializations for performance in light-limited environments. Despite representing the greatest ecological diversity and species richness in Chiroptera, Neotropical lineages have been undersampled in molecular studies, limiting the potential for identifying signatures of selection on visual genes associated with differences in bat ecology. Here, we investigated how diverse ecological pressures mediate long-term shifts in selection upon long-wavelength () and short-wavelength () opsins, photosensitive cone pigments that form the basis of colour vision in most mammals, including bats. We used codon-based likelihood clade models to test whether ecological variables associated with reliance on visual information (e.g. echolocation ability and diet) or exposure to varying light environments (e.g. roosting behaviour and foraging habitat) mediated shifts in evolutionary rates in bat cone opsin genes. Using additional cone opsin sequences from newly sequenced eye transcriptomes of six Neotropical bat species, we found significant evidence for different ecological pressures influencing the evolution of the cone opsins. While is evolving under significantly lower constraint in highly specialized high-duty cycle echolocating lineages, which have enhanced sonar ability to detect and track targets, variation in constraint was significantly associated with foraging habitat, exhibiting elevated rates of evolution in species that forage among vegetation. This suggests that increased reliance on echolocation as well as the spectral environment experienced by foraging bats may differentially influence the evolution of different cone opsins. Our study demonstrates that different ecological variables may underlie contrasting evolutionary patterns in bat visual opsins, and highlights the suitability of clade models for testing ecological hypotheses of visual evolution.

show abstract

“…The dim-light visual pigment rhodopsin (RH1/RHO) is an excellent model for understanding how both ecological variables and biophysical pleiotropy may interact to determine the availability of functional evolutionary solutions for environmental challenges ( Kojima et al, 2017 ; Gozem et al, 2012 ; Dungan and Chang, 2017 ; Castiglione et al, 2018 ). Spectral tuning mutations that shift the RH1 wavelength of maximum absorbance (λ MAX ) can adapt dim-light vision to a remarkable range of spectral conditions across aquatic and terrestrial visual ecologies ( Hunt et al, 2001 ; Hauser and Chang, 2017a ; Dungan et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

Castiglione

Chang

2018

eLife

View full text Add to dashboard Cite

Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity.

show abstract

Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms

Abstract: Convergent evolution in response to

Cited by 20 publications

References 97 publications

Convergent phenotypic evolution of the visual system via different molecular routes: How Neotropical cichlid fishes adapt to novel light environments

Convergent phenotypic evolution of the visual system via different molecular routes: How Neotropical cichlid fishes adapt to novel light environments

The role of ecological factors in shaping bat cone opsin evolution

Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

Contact Info

Product

Resources

About