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      Bentho-Pelagic Divergence of Cichlid Feeding Architecture Was Prodigious and Consistent during Multiple Adaptive Radiations within African Rift-Lakes

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          Abstract

          Background

          How particular changes in functional morphology can repeatedly promote ecological diversification is an active area of evolutionary investigation. The African rift-lake cichlids offer a calibrated time series of the most dramatic adaptive radiations of vertebrate trophic morphology yet described, and the replicate nature of these events provides a unique opportunity to test whether common changes in functional morphology have repeatedly facilitated their ecological success.

          Methodology/Principal Findings

          Specimens from 87 genera of cichlid fishes endemic to Lakes Tanganyka, Malawi and Victoria were dissected in order to examine the functional morphology of cichlid feeding. We quantified shape using geometric morphometrics and compared patterns of morphological diversity using a series of analytical tests. The primary axes of divergence were conserved among all three radiations, and the most prevalent changes involved the size of the preorbital region of the skull. Even the fishes from the youngest of these lakes (Victoria), which exhibit the lowest amount of skull shape disparity, have undergone extensive preorbital evolution relative to other craniofacial traits. Such changes have large effects on feeding biomechanics, and can promote expansion into a wide array of niches along a bentho-pelagic ecomorphological axis.

          Conclusions/Significance

          Here we show that specific changes in trophic anatomy have evolved repeatedly in the African rift lakes, and our results suggest that simple morphological alterations that have large ecological consequences are likely to constitute critical components of adaptive radiations in functional morphology. Such shifts may precede more complex shape changes as lineages diversify into unoccupied niches. The data presented here, combined with observations of other fish lineages, suggest that the preorbital region represents an evolutionary module that can respond quickly to natural selection when fishes colonize new lakes. Characterizing the changes in cichlid trophic morphology that have contributed to their extraordinary adaptive radiations has broad evolutionary implications, and such studies are necessary for directing future investigations into the proximate mechanisms that have shaped these spectacular phenomena.

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          Most cited references37

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          Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.

          Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.
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            Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences.

            Lake Victoria, together with its satellite lakes, harbours roughly 200 endemic forms of cichlid fishes that are classified as 'haplochromines' and yet the lake system is less than a million years old. This 'flock' has attracted attention because of the possibility that it evolved within the lake from one ancestral species and that biologists are thus presented with a case of explosive evolution. Within the past decade, however, morphology has increasingly emphasized the view that the flock may be polyphyletic. We sequenced up to 803 base pairs of mitochondrial DNA from 14 representative Victorian species and 23 additional African species. The flock seems to be monophyletic, and is more akin to that from Lake Malawi than to species from Lake Tanganyika; in addition, it contains less genetic variation than does the human species, and there is virtually no sharing of mitochondrial DNA types among species. These results confirm that the founding event was recent.
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              Divergent sexual selection enhances reproductive isolation in sticklebacks.

              J Boughman (2001)
              Sexual selection may facilitate speciation because it can cause rapid evolutionary diversification of male mating signals and female preferences. Divergence in these traits can then contribute to reproductive isolation. The sensory drive hypothesis predicts that three mechanisms underlie divergence in sexually selected traits: (1) habitat-specific transmission of male signals; (2) adaptation of female perceptual sensitivity to local ecological conditions; and (3) matching of male signals to female perceptual sensitivity. I test these mechanisms in threespine sticklebacks (Gasterosteus spp.) that live in different light environments. Here I show that female perceptual sensitivity to red light varies with the extent of redshift in the light environment, and contributes to divergent preferences. Male nuptial colour varies with environment and is tuned to female perceptual sensitivity. The extent of divergence among populations in both male signal colour and female preference for red is correlated with the extent of reproductive isolation in these recently diverged species. These results demonstrate that divergent sexual selection generated by sensory drive contributes to speciation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                8 March 2010
                : 5
                : 3
                : e9551
                Affiliations
                [1 ]Department of Biology, Syracuse University, Syracuse, New York, United States of America
                [2 ]School of Dental Medicine, University of Connecticut, Storrs, Connecticut, United States of America
                University of Hull, United Kingdom
                Author notes

                Conceived and designed the experiments: WJC KJP RCA. Performed the experiments: WJC KJP AM BK AMM RCA. Analyzed the data: WJC KJP AM BK AMM RCA. Contributed reagents/materials/analysis tools: RCA. Wrote the paper: WJC KJP AM BK AMM RCA.

                Article
                09-PONE-RA-12704R2
                10.1371/journal.pone.0009551
                2833203
                20221400
                25ee344d-97f7-4ef6-a018-e89cf2a8f228
                Cooper 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.
                History
                : 4 September 2009
                : 9 February 2010
                Page count
                Pages: 13
                Categories
                Research Article
                Evolutionary Biology
                Ecology/Evolutionary Ecology
                Marine and Aquatic Sciences/Evolutionary Biology

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                Uncategorized

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