The evolution of the extraordinary inflation mechanism of pufferfishes was studied in the light of an independently derived phylogenetic hypothesis of tetraodontiform fishes. Inflation behavior is found in all members of the puffer sister taxa Tetraodontidae and Diodontidae. However, most other tetraodontiform fishes exhibit two functionally similar behaviors. All taxa exhibit a "coughing" behavior and, with the exception of the sister-group to all other tetraodontiforms, represented by the Triacanthidae, all lineages "blow" strong jets of water out of their mouth to excavate prey. Functional specializations associated with the three behaviors were identified from anatomical analyses and electromyographic recordings of muscle activity in representatives of the major lineages of the order. The phylogenetic distribution of the three buccal compression behaviors and their functional bases indicates the following: (1) the evolution of inflation behavior involved major structural modifications of the head that function in a novel mechanism that links depression of the floor of the mouth to posterior expansion of the buccal cavity; (2) the contraction patterns of four key head muscles used in the three behaviors are generally similar both across behaviors and taxa; (3) however, the distribution of the two significant modifications of muscle activity are consistent with the hypothesis that the three behaviors represent a transformation series from coughing to water blowing to inflation. The motor pattern for water blowing is a slightly modified version of that seen in coughing, and the inflation motor pattern retains the blowing specialization and adds a single additional modification. The convergent evolution of a poorly developed inflation behavior in at least one genus of filefish provides evidence that tetraodontiform fishes are predisposed to the evolution of this unusual defensive behavior. The presence of a well developed water-blowing behavior in most tetraodontiform lineages may represent an intermediate functional specialization that increased the probability of the evolution of inflation.
Keywords: Balistes; Chilomycterus; Monacanthus; Sphoeroides; Tetraodontiformes; Triacanthus.; electromyography; inflation; transformation series.
© 1997 The Society for the Study of Evolution.