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A novel resource polymorphism in fish, driven by differential bottom environments: an example from an ancient lake in Japan.

Komiya T, Fujita S, Watanabe K - PLoS ONE (2011)

Bottom Line: Genetic analyses based on mitochondrial and nuclear microsatellite DNA data revealed no clear genetic differentiation among local populations within/between the gudgeon species.Although the morphogenetic factors that contribute to morphological divergence remain unclear, our results suggest that the gudgeon populations in Lake Biwa show a state of resource polymorphism associated with differences in the bottom environment.This is a novel example of resource polymorphism in fish within an Asian ancient lake, emphasizing the importance and generality of feeding adaptation as an evolutionary mechanism that generates morphological diversification.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Science, Kyoto University, Kyoto, Japan. komiya@terra.zool.kyoto-u.ac.jp

ABSTRACT
Divergent natural selection rooted in differential resource use can generate and maintain intraspecific eco-morphological divergence (i.e., resource polymorphism), ultimately leading to population splitting and speciation. Differing bottom environments create lake habitats with different benthos communities, which may cause selection in benthivorous fishes. Here, we document the nature of eco-morphological and genetic divergence among local populations of the Japanese gudgeon Sarcocheilichthys (Cyprinidae), which inhabits contrasting habitats in the littoral zones (rocky vs. pebbly habitats) in Lake Biwa, a representative ancient lake in East Asia. Eco-morphological analyses revealed that Sarcocheilichthys variegatus microoculus from rocky and pebbly zones differed in morphology and diet, and that populations from rocky environments had longer heads and deeper bodies, which are expected to be advantageous for capturing cryptic and/or attached prey in structurally complex, rocky habitats. Sarcocheilichthys biwaensis, a rock-dwelling specialist, exhibited similar morphologies to the sympatric congener, S. v. microoculus, except for body/fin coloration. Genetic analyses based on mitochondrial and nuclear microsatellite DNA data revealed no clear genetic differentiation among local populations within/between the gudgeon species. Although the morphogenetic factors that contribute to morphological divergence remain unclear, our results suggest that the gudgeon populations in Lake Biwa show a state of resource polymorphism associated with differences in the bottom environment. This is a novel example of resource polymorphism in fish within an Asian ancient lake, emphasizing the importance and generality of feeding adaptation as an evolutionary mechanism that generates morphological diversification.

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Sampling localities and mtDNA haplotype group frequencies of Sarcocheilichthys in Lake Biwa, Japan (A).Northern and eastern rocky zones are shaded in orange. Statistical parsimony network for mtDNA of Sarcocheilichthys (B). The areas of the circles are proportional to haplotype frequency. A dashed line indicates an alternative connection (loop). In both (A) and (B), each clade is shown in the same color. Sample codes correspond to those in Table 1.
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pone-0017430-g001: Sampling localities and mtDNA haplotype group frequencies of Sarcocheilichthys in Lake Biwa, Japan (A).Northern and eastern rocky zones are shaded in orange. Statistical parsimony network for mtDNA of Sarcocheilichthys (B). The areas of the circles are proportional to haplotype frequency. A dashed line indicates an alternative connection (loop). In both (A) and (B), each clade is shown in the same color. Sample codes correspond to those in Table 1.

Mentions: For the morphometric and molecular analyses, we collected samples of S. biwaensis and S. v. microoculus from the entire shoreline of Lake Biwa between 2002 and 2007 (Figure 1A; Table 1). We identified the two groups primarily based on body color [20], [21]. Specimens from the collection at the Lake Biwa Museum, Shiga Prefecture, Japan, caught between 1974 and 1993, were also included among our samples. The total numbers of samples used in morphometric analyses were 508 and 370 from a total of 15 sites for head and body shape analyses, respectively, whereas for the molecular analyses, we used 207 and 181 samples from a total of 14 sites for the mtDNA and microsatellite analyses, respectively (see Table 1 for details). These local samples were, for convenience, regarded as “local populations.” Five rocky and ten pebbly local populations of S. v. microoculus were labeled using the sample codes R1–5 and P1–10, respectively. For S. biwaensis, because of the small sample size per site, samples from northern (R1–2, exceptionally captured from P1 and P10) and eastern (R3 and R5) rocky zones were pooled under the codes BN and BE, respectively. We judged whether each site represented a rocky or pebbly environment according to quantitative data on substratum constitutions reported by Nishino [24]; rocky habitats are restricted in relatively small areas of northern and eastern parts (Figure 1A).


A novel resource polymorphism in fish, driven by differential bottom environments: an example from an ancient lake in Japan.

Komiya T, Fujita S, Watanabe K - PLoS ONE (2011)

Sampling localities and mtDNA haplotype group frequencies of Sarcocheilichthys in Lake Biwa, Japan (A).Northern and eastern rocky zones are shaded in orange. Statistical parsimony network for mtDNA of Sarcocheilichthys (B). The areas of the circles are proportional to haplotype frequency. A dashed line indicates an alternative connection (loop). In both (A) and (B), each clade is shown in the same color. Sample codes correspond to those in Table 1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3046152&req=5

pone-0017430-g001: Sampling localities and mtDNA haplotype group frequencies of Sarcocheilichthys in Lake Biwa, Japan (A).Northern and eastern rocky zones are shaded in orange. Statistical parsimony network for mtDNA of Sarcocheilichthys (B). The areas of the circles are proportional to haplotype frequency. A dashed line indicates an alternative connection (loop). In both (A) and (B), each clade is shown in the same color. Sample codes correspond to those in Table 1.
Mentions: For the morphometric and molecular analyses, we collected samples of S. biwaensis and S. v. microoculus from the entire shoreline of Lake Biwa between 2002 and 2007 (Figure 1A; Table 1). We identified the two groups primarily based on body color [20], [21]. Specimens from the collection at the Lake Biwa Museum, Shiga Prefecture, Japan, caught between 1974 and 1993, were also included among our samples. The total numbers of samples used in morphometric analyses were 508 and 370 from a total of 15 sites for head and body shape analyses, respectively, whereas for the molecular analyses, we used 207 and 181 samples from a total of 14 sites for the mtDNA and microsatellite analyses, respectively (see Table 1 for details). These local samples were, for convenience, regarded as “local populations.” Five rocky and ten pebbly local populations of S. v. microoculus were labeled using the sample codes R1–5 and P1–10, respectively. For S. biwaensis, because of the small sample size per site, samples from northern (R1–2, exceptionally captured from P1 and P10) and eastern (R3 and R5) rocky zones were pooled under the codes BN and BE, respectively. We judged whether each site represented a rocky or pebbly environment according to quantitative data on substratum constitutions reported by Nishino [24]; rocky habitats are restricted in relatively small areas of northern and eastern parts (Figure 1A).

Bottom Line: Genetic analyses based on mitochondrial and nuclear microsatellite DNA data revealed no clear genetic differentiation among local populations within/between the gudgeon species.Although the morphogenetic factors that contribute to morphological divergence remain unclear, our results suggest that the gudgeon populations in Lake Biwa show a state of resource polymorphism associated with differences in the bottom environment.This is a novel example of resource polymorphism in fish within an Asian ancient lake, emphasizing the importance and generality of feeding adaptation as an evolutionary mechanism that generates morphological diversification.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Science, Kyoto University, Kyoto, Japan. komiya@terra.zool.kyoto-u.ac.jp

ABSTRACT
Divergent natural selection rooted in differential resource use can generate and maintain intraspecific eco-morphological divergence (i.e., resource polymorphism), ultimately leading to population splitting and speciation. Differing bottom environments create lake habitats with different benthos communities, which may cause selection in benthivorous fishes. Here, we document the nature of eco-morphological and genetic divergence among local populations of the Japanese gudgeon Sarcocheilichthys (Cyprinidae), which inhabits contrasting habitats in the littoral zones (rocky vs. pebbly habitats) in Lake Biwa, a representative ancient lake in East Asia. Eco-morphological analyses revealed that Sarcocheilichthys variegatus microoculus from rocky and pebbly zones differed in morphology and diet, and that populations from rocky environments had longer heads and deeper bodies, which are expected to be advantageous for capturing cryptic and/or attached prey in structurally complex, rocky habitats. Sarcocheilichthys biwaensis, a rock-dwelling specialist, exhibited similar morphologies to the sympatric congener, S. v. microoculus, except for body/fin coloration. Genetic analyses based on mitochondrial and nuclear microsatellite DNA data revealed no clear genetic differentiation among local populations within/between the gudgeon species. Although the morphogenetic factors that contribute to morphological divergence remain unclear, our results suggest that the gudgeon populations in Lake Biwa show a state of resource polymorphism associated with differences in the bottom environment. This is a novel example of resource polymorphism in fish within an Asian ancient lake, emphasizing the importance and generality of feeding adaptation as an evolutionary mechanism that generates morphological diversification.

Show MeSH