Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective.
The fish fauna of the continental shelf of the Southern Ocean is dominated by a single sub-order of Perciformes, the Notothenioidei, which have unusually large diameter skeletal muscle fibres. We tested the hypothesis that in fast myotomal muscle a high maximum fibre diameter (FD(max)) was related to a reduction in the number of muscle fibres present at the end of the recruitment phase of growth. We also hypothesized that the maximum fibre number (FN(max)) would be negatively related to body size, and that both body size and size-corrected FN(max) would show phylogenetic signal (tendency for related species to resemble each other). Finally, we estimated ancestral values for body size and FN(max). A molecular phylogeny was constructed using 12S mitochondrial rRNA sequences. A total of 16 species were studied from the Beagle Channel, Tierra del Fuego (5-11 degrees C), Shag Rocks, South Georgia (0.5-4 degrees C), and Adelaide Island, Antarctic Peninsula (-1.5 to 0.5 degrees C). The absence of muscle fibres of less than 10 micro m diameter was used as the criterion for the cessation of fibre recruitment. FD(max) increased linearly with standard length (SL), reaching 500-650 micro m in most species. Maximum body size was a highly significant predictor of species variation in FN(max), and both body size and size-corrected FN(max) showed highly significant phylogenetic signal (P<0.001). Estimates of trait values at nodes of the maximum likelihood phylogenetic tree were consistent with a progressive reduction in fibre number during part of the notothenioid radiation, perhaps serving to reduce basal energy requirements to compensate for the additional energetic costs of antifreeze production. For example, FN(max) in Chaenocephalus aceratus (12 700+/-300, mean +/- S.E.M., N=18) was only 7.7% of the value found in Eleginops maclovinus (164 000+/-4100, N=17), which reaches a similar maximum length (85 cm). Postembryonic muscle fibre recruitment in teleost fish normally involves stratified followed by mosaic hyperplasia. No evidence for this final phase of growth was found in two of the most derived families (Channichthyidae and Harpagiferidae). The divergence of the notothenioids in Antarctica after the formation of the Antarctic Polar Front and more recent dispersal north would explain the high maximum diameter and low fibre number in the derived sub-Antarctic notothenioids. These characteristics of notothenioids may well restrict their upper thermal tolerance, particularly for Champsocephalus esox and similar Channichthyids that lack respiratory pigments.
Johnston
Ian A
IA
Gatty Marine Laboratory, Division of Environmental and Evolutionary Biology, School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB, Scotland, UK. iaj@st-and.ac.uk
Fernández
Daniel A
DA
Calvo
Jorge
J
Vieira
Vera L A
VL
North
Anthony W
AW
Abercromby
Marguerite
M
Garland
Theodore
T
D000220:Adaptation, Biological / Q000502:physiology*; D000818:Animals; D000864:Antarctic Regions; D001483:Base Sequence; D001824:Body Constitution / Q000502:physiology; D017931:DNA Primers; D006652:Histological Techniques; D016013:Likelihood Functions; D008969:Molecular Sequence Data; D018485:Muscle Fibers, Skeletal / Q000502:physiology*; D010473:Perciformes / Q000235:genetics* / Q000254:growth & development / Q000502:physiology*; D010802:Phylogeny; D012313:RNA / Q000235:genetics; D000077278:RNA, Mitochondrial
D017931:DNA Primers; D000077278:RNA, Mitochondrial; D012313:RNA