The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai

Citation
Jb. Graham et Ka. Dickson, The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai, ZOOL J LINN, 129(4), 2000, pp. 419-466
Citations number
99
Language
INGLESE
art.tipo
Article
Categorie Soggetti
Animal Sciences
Journal title
ZOOLOGICAL JOURNAL OF THE LINNEAN SOCIETY
ISSN journal
0024-4082 → ACNP
Volume
129
Issue
4
Year of publication
2000
Pages
419 - 466
Database
ISI
SICI code
0024-4082(200008)129:4<419:TEOTLA>2.0.ZU;2-F
Abstract
Two significant functional differences-a more anterior and internally posit ioned red myotomal muscle mass and modification of the red-muscle vascular supply to form countercurrent heat exchangers-distinguish the tunas (tribe Thunnini) from other species in the teleost family Scombridae. Neither of t hese characteristics is found in the bonitos (tribe Sardini), the sister gr oup to the Thunnini. The most recent scombrid classification places the sle nder tuna, Allothunnus fallai, in the tribe Sardini, but some earlier studi es suggested that this species should be a member of the Thunnini. Allothun nus fallai does not possess the lateral subcutaneous arteries and veins or the lateral heat-exchanging retia typical of tunas. However, we have found that this species has a highly modified central circulation (dorsal aorta, post cardinal vein, and associated branch vessels) similar to the central h eat-exchanging retia of certain tunas, an enlarged haemal arch to accommoda te this structure, and the anterior, internal placement of red muscle chara cteristic of tunas. With these new characters, phylogenetic reconstructions based on parsimony place A. fallai as the sister taxon to the tunas, estab lish that it is the most basal tuna species, and support the hypothesis tha t the derivation of tunas from a bonito-like ancestor occurred through sele ction for an integrated set of characteristics affecting locomotion and end othermy. The major features of this hypothesis are as follows. (1) Selectio n for continuous, steady, and efficient swimming resulted in changes in bod y shape (the result of enlargement of the anterior myotomes, the anterior a nd internal shift of red muscle, and a narrowing of the caudal peduncle) wh ich increased streamlining and led to the adoption of the thunniform swimmi ng mode unique to the tunas. (2) Alterations in blood supply necessitated b y the anterior shift in red muscle led to the interdigitation of numerous a rterial and venous branches which set the stage for heat conservation. (3) The evolution of endothermy, together with thunniform swimming, contributed significantly to the ecological radiation and diversification of tunas dur ing the Early Tertiary Period. Our studies of A. fallai thus suggest that t he shift in red muscle position and changes in central circulation preceded the evolution of red-muscle endothermy. Co-evolutionary changes in red mus cle quantity and distribution and in vascular specializations for heat cons ervation have led to different macroevolutionary trajectories among the now five genera and 14 tuna species of tunas and appear to reflect the influen ce of changing paleocological and paleoceanographic conditions, including c ooling, that occurred in the Tertiary. (C) 2000 The Linnean Society of Lond on.