Tentando elucidar a evolução da diversidade de pigmentação dos olhos em ciclídeos

The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity

Christopher M. Hofmann1#*, Kelly E. O'Quin1#, N. Justin Marshall2, Thomas W. Cronin3, Ole Seehausen4,5, Karen L. Carleton1

1 Department of Biology, University of Maryland, College Park, Maryland, United States of America,

2 Sensory Neurobiology Group, School of Biomedical Sciences University of Queensland, St. Lucia, Queensland, Australia,

3 Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland, United States of America,

4 Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland,

5 Eawag, Swiss Federal Institute for Aquatic Science and Technology, Centre of Ecology, Evolution and Biogeochemistry, Kastanienbaum, Switzerland

Abstract Top

A major goal of evolutionary biology is to unravel the molecular genetic mechanisms that underlie functional diversification and adaptation. We investigated how changes in gene regulation and coding sequence contribute to sensory diversification in two replicate radiations of cichlid fishes. In the clear waters of Lake Malawi, differential opsin expression generates diverse visual systems, with sensitivities extending from the ultraviolet to the red regions of the spectrum. These sensitivities fall into three distinct clusters and are correlated with foraging habits. In the turbid waters of Lake Victoria, visual sensitivity is constrained to longer wavelengths, and opsin expression is correlated with ambient light. In addition to regulatory changes, we found that the opsins coding for the shortest- and longest-wavelength visual pigments have elevated numbers of potentially functional substitutions. Thus, we present a model of sensory evolution in which both molecular genetic mechanisms work in concert. Changes in gene expression generate large shifts in visual pigment sensitivity across the collective opsin spectral range, but changes in coding sequence appear to fine-tune visual pigment sensitivity at the short- and long-wavelength ends of this range, where differential opsin expression can no longer extend visual pigment sensitivity.

Author Summary Top

The molecular mechanisms that generate biodiversity remain largely elusive. We examined how two of these mechanisms, changes in gene expression and changes in gene coding sequence, have generated an incredibly diverse set of visual systems in rapidly speciating African cichlids. We found large differences in cone opsin gene expression among cichlids inhabiting the clear waters of Lake Malawi. These changes are likely to have strong influences on retinal sensitivity and appear to be driven primarily by different foraging needs. Cichlids inhabiting the turbid waters of Lake Victoria, however, only expressed a subset of their opsin genes and variation in gene expression appears to by driven primarily by the spectrum of environmental light. When we compared the sequences of these opsin genes, we found greater variation in the genes at the ultraviolet and red edges of the sensitivity range. Taken together these findings suggest that changes in gene expression and coding sequence can be complementary and work in concert to generate changes in sensory systems. Because of their correlation with ecological factors, these changes are also likely to be adaptive and to have played a role in generating the tremendous diversity of cichlids in these two lakes.

Citation: Hofmann CM, O'Quin KE, Marshall NJ, Cronin TW, Seehausen O, et al. (2009) The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity. PLoS Biol 7(12): e1000266. doi:10.1371/journal.pbio.1000266

Academic Editor: Mohamed A. F. Noor, Duke University, United States of America

Received: April 22, 2009; Accepted: November 12, 2009; Published: December 22, 2009

Copyright: © 2009 Hofmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: Funding for this work was provided to KC by the University of Maryland and the National Science Foundation, IBN 0131285, 0654076, 0841270; and to OS by the Swiss National Science Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

* E-mail: chofma1@umd.edu

# These authors contributed equally to this work.

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