Out of place and out of time – towards a more integrated approach to heterochrony

Heterochrony (changes in the relative timing of development between species) has been studied almost exclusively using morphological characters, with a focus on changes in size and shape (as a surrogate for time) between ancestral species and their descendents. Such an approach is restrictive in that it precludes the investigation of heterochronies in other, non-morphological traits and, therefore, hampers a more integrated approach to heterochrony. Such an integrated approach, where cellular, molecular and genetic approaches are used within a comparative phylogenetic framework to investigate developmental sequences, has been advocated by workers such as Smith and Raff. Here we suggest that equal emphasis should be given to the importance of physiological and ecological mechanisms that relate to changes in developmental sequence. Reviews of the history and status of physiological and ecological heterochrony reveal several examples for each, although progress has been hampered to some degree by a lack of recognition of physiological heterochrony and a lack of mechanistic understanding (heterochronies in evolutionary ecology). What emerges is that each discipline potentially brings something quite different, and complementary, to the study of heterochrony. The emergence of physiological heterochrony has arguably put the emphasis back on the object of selection and how the developing organism works: studies relating ecology and heterochrony have sought to establish whether or not there is an adaptive basis to altered sequences. We propose that any future studies of heterochrony should seek to exploit these different strengths rather than see them as merely complementary approaches.