Physiological Progenesis in Cephalopod Molluscs

The coleoid cephalopods (cuttlefish, squid and octopus) arose from their shelled ancestors during the late Devonian; they diversified in the Jurassic but did not radiate substantially until the Tertiary. Since then they have coevolved with the fish (1). Squid are less efficient energetically than fish (2) but have survived alongside them by evolving highly opportunistic reproductive and feeding strategies (3, 4) as well as rapid jetting and inking for escape and defense. Little is known about the life history strategies of the fossil forms, but the only surviving shelled cephalopods, the nautiluses, have relatively long life spans and are iteroparous; that is, in common with most members of other molluscan classes, they breed more than once during their lives. In contrast, all other living cephalopods are generally short lived (usually 1 year) and have monocyclic reproduction and a semelparous life history. The short-lived semelparous coleoids are typified by the mid-latitude ommastrephid squid which provide the basic model considered here. This family is relatively primitive and biologically well known. Its members are essentially monocyclic, but some species may spawn their eggs in batches (5, 6) although there is no evidence of this in laboratory spawnings (7). Most loliginid squid, at least in temperate seas, have a life cycle similar to that of the ommastrephids, despite having different spawning habits. A comparison of the lifetime energetics and growth pattern of benthic, iteroparous molluscs with those of the pelagic, semelparous ommastrephids shows that, although some squid may attain a length of 1 m or more, the allocation of their energy resource among growth components is essentially characteristic of the early life, especially the first year, of iteroparous forms. The life-time energy budget of these squid thus seems to have evolved by physiological progenesis, a process in which maturation is accelerated while other aspects of the physiology are more typical of the juvenile.