Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective

Abstract

SUMMARY 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 (FDmax) 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 (FNmax) would be negatively related to body size,and that both body size and size-corrected FNmax would show phylogenetic signal (tendency for related species to resemble each other). Finally, we estimated ancestral values for body size and FNmax. 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°C), Shag Rocks, South Georgia(0.5-4°C), and Adelaide Island, Antarctic Peninsula (-1.5 to 0.5°C). The absence of muscle fibres of less than 10 μm diameter was used as the criterion for the cessation of fibre recruitment. FDmaxincreased linearly with standard length (SL), reaching 500-650 μm in most species. Maximum body size was a highly significant predictor of species variation in FNmax, and both body size and size-corrected FNmax 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, FNmax 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.

Loss of muscle fibres in a landlocked dwarf Atlantic salmon population

“…If correct, our hypothesis may help to explain much of the variation in muscle fibre number associated with changes in body size and temperature during the adaptive radiation of teleosts ( Johnston et al 2003b).…”

Fishes of southern South America: a story driven by temperature

“…Similar long post-prandial times and not so high oxygen consumption values have been found in sub-Antarctic notothenioids (F. Vanella, personal communication). Johnston et al (2003) have shown that the radiation of Antarctic and sub-Antarctic notothenioids was associated with a progressive decrease in the body size-specific maximum number of fast fibers in the myotomal muscles of the more derived species, but not with a reduction in body size. Thus, if fiber sizebut not body size-is reduced, there should be an increase in the size of the muscle fibers.…”

“…Thus, if fiber sizebut not body size-is reduced, there should be an increase in the size of the muscle fibers. In actual fact, this group does have unusually large muscle fibers, with diameters that can reach 100 lm in slow muscle and 500 lm in fast muscle (Smialowska and Kilarsky 1981;Dunn et al 1989;Battram and Johnston 1991;Fernández et al 2000;Johnston et al 2003;Fernán-dez et al 2005). This characteristic imposes obvious constraints in terms of oxygen diffusion and important metabolites, such as ATP, restricting muscle fiber size at least in aerobic fibers (slow twitch muscle fibers).…”

“…Large muscle fibers could have been favored in the evolution of notothenioids, since the decrease in the fiber surface to volume ratio will decrease the cost of maintaining ion homeostasis in these fibers. This idea, called the 'optimal fiber size hypothesis', was proposed by Johnston et al (2003Johnston et al ( , 2004 for notothenioids and Arctic char evolution and by Kinsey et al (2005) for blue crabs.…”

“…, ecological interactions (Milano et al 2002(Milano et al , 2006, alien species (Macchi et al 1999(Macchi et al , 2007, human impacts (Pascual et al 2002;Ortubay et al 2006), phylogeography, and molecular phylogeny (Johnston et al 2003;Near et al 2004;Zattara and Premoli 2005;Ruzzante et al 2006).…”