Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective
Ian A. Johnston1,*,
Daniel A. Fernández1,
,
Jorge Calvo2,
Vera L. A. Vieira1,
Anthony W. North3,
Marguerite Abercromby1 and
Theodore Garland, Jr4
1 Gatty Marine Laboratory, Division of Environmental and Evolutionary Biology,
School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB,
Scotland, UK
2 Centro Austral de Investigaciones Cientificas (CADIC), Consejo Nacional de
Investigaciones Cientificas y Tecnicas (CONICET) CC92, Ushuaia, 9410, Tierra
del Fuego, Argentina
3 British Antarctic Survey, High Cross, Madingley Road, Cambridge, CB3 OET,
UK
4 Department of Biology, University of California, Riverside, CA 92521,
USA
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Fig. 1. Sample sites in relation to the Polar Frontal Zone and summer and winter
sea surface temperatures represented by the mean of satellite observations
between 1971 and 2001 for February and September.
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Fig. 2. Phases of growth observed in the myotomal muscle of Antarctic and
sub-Antarctic notothenioid fish. (A–G) Transverse sections through the
trunk stained with Haematoxylin–Eosin (A) Section from Notothenia
coriiceps, 11.2 cm standard length (SL), stained with the
antibody S58, showing the presence of a superficial layer of slow muscle
fibres (arrows) dorsal to the major horizontal septum. (B) Trematomus
newnesi, 13.3 cm SL, section stained with S58 showing the slow
muscle fibres adjacent to the lateral line nerve (arrows). The fast muscle
fibres were counterstained with Haematoxylin–Eosin. (C) Dorsal region of
the trunk in a juvenile Notothenia coriiceps, 6.0 cm SL. The
arrowheads indicate zones of stratified hyperplasia containing fibres of
smaller diameter than the surrounding tissue. (D) The start of mosaic
hyperplasia (arrowheads) in the fast muscle of a juvenile Notothenia
coriiceps, 6.7 cm SL. Note that small diameter satellite fibres
are not uniformly distributed through the field of view. (E) The pattern of
fibre diameters characteristic of mosaic hyperplasia was still present in
E. maclovinus of 37.5 cm SL. (F) Active mosaic hyperplasia
(arrowheads) in the fast muscle of a juvenile Eleginops maclovinus,
4.7 cm SL. (G) The smallest specimen of Paranotothenia
magellanica captured, 9.3 cm SL, showed a mosaic pattern of
fibre diameters (arrowheads). s, slow muscle; f, fast muscle; sk, skin; ms,
myosepta. Scale bars, 200 µm (A–C,E); 100 µm (D,F,G).
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Fig. 8. Maximum likelihood phylogenetic tree estimated from 12S mitochondrial rRNA
sequences and the trait values for the final number of fast muscle fibres
(FNmax) for the notothenioid fishes studied using Phylip.
Values are means ± S.E.M. (number of
individuals). The bootstrap support values obtained from the Phylip analysis
are shown italicised in parentheses by the nodes (see text for details). The
branch lengths and node heights for the tree are given in the Appendix. The
size of the fish gives some indication of their relative sizes, but they are
not drawn to scale. The locomotory habit of each species is also shown: D,
demersal; D/P, demerso-pelagic and P, pelagic. The colours on the right-hand
side show the geographical zone of capture for each species: Beagle Channel
(green), Shag Rocks, South Georgia (light blue) and Antarctic Peninsula (dark
blue). The colours on the left-hand side indicate the current taxonomic
families, some of which are not monophyletic.
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Fig. 3. Phases of growth observed in the myotomal muscle of Antarctic and
sub-Antarctic notothenioid fish that have a relatively low final muscle fibre
number. (A) Transverse section through the trunk stained with
Haematoxylin–Eosin from an adult icefish Chaenocephalus
aceratus, 27.6 cm standard length (SL). Note the relatively
uniform distribution of large diameter (approx. 200 µm) muscle fibres. (B)
Transverse section of a region of fast muscle fibres from an adult
Notothenia coriiceps, 35.5 cm SL, stained with Scarab Red to
visualise collagen fibrils. The arrowheads show the apparent splitting of a
fibre into smaller daughter fibres each surrounded by a connective tissue
sheath. (C) Transverse section of a region of fast muscle fibres from an adult
Patagonotothen longipes sp. (27.8 cm SL) showing the
apparent splitting of a fibre into smaller daughter fibres. Arrowheads
indicate the position of myonuclei. ms, myosepta. Scale bars, 200 µm (A,B);
100 µm (C).
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Fig. 4. The distribution of muscle fibre diameters in relation to fish standard
length (SL, cm) in the fast myotomal muscle of (A) Eleginops
maclovinus and (B) Patagonotothen tessellata. Smooth
distributions were fitted to 1000 measurements of muscle fibre diameter using
a kernel function. Each dotted line represents an individual fish. The
coloured lines represent the smallest (red), the largest (blue) and an
intermediate size (green) fish, of indicated SL.
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Fig. 5. The relationship between the estimated maximum fast muscle fibre diameter
and standard length within nine species of Notothenioid fishes from the
Southern Ocean and Patagonian shelf. (A) Antarctic Peninsula, Notothenia
coriiceps (open squares); Shag Rocks, Dissosticus eleginoides
(open circles); Tierra del Fuego, Eleginops maclovinus (filled
circles), Patagonotothen tessellata (open triangles), P.
longipes sp. (inverted filled triangles) and P. sima (filled
squares). (B) Shag rocks, Icefishes Chaenocephalus aceratus (open
triangles), Champsocephalus gunnari (open squares); Tierra del Fuego,
Paratonothenia magellanica (closed circles).
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Fig. 6. (A–C). The relationship between the number of muscle fibres and the
total cross-sectional area (TCA) of fast muscle at 0.7 standard length
(SL). (A) Eleginops maclovinus, (B) Patagonotothen
tessellata and (C) Notothenia coriiceps. The broken lines
represent the estimate of FNmax.
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Fig. 7. The relationship between log10 maximum fibre number
(FNmax; data from Fig.
8) and log10 maximum standard length
(SLmax; data from Table
1) among 16 species of notothenioid fishes from Tierra del Fuego
(filled circles), Shag Rocks, South Georgia (open triangles) and the Antarctic
Peninsula (open circles). A conventional least-squares linear regression was
fitted to the data. The equation was:
log10FNmax=2.53+log10SLmaxx1.12
(F1,14=30.8, P<0.0001;
r2=0.69).
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© The Company of Biologists Ltd 2003
