Generic aspects of molluscan shell morphogenesis: theoretical, experimental and comparative approaches

Abstract

How an embryo develops its particular form during ontogeny and how shape changes through evolutionary time are two closely linked questions. An approach to these issues, mainly inspired by D'Arcy Thompson's work, is to highlight the 'laws of form', that is how developmental systems determine the variation of organismal forms on short and long time scales. During the last decades, theoretical models of morphogenesis have allowed the identification of some of these rules from experimentally well-studied developmental systems. Molluscs are also well suited to address the relationships between evolution and development. The preservation of the ontogeny of the shell due to its accretionary growth and the excellent fossil record in this group are undeniable advantages. Also, molluscan shell shape and growth have been the focus of extensive theoretical work, revealing the regularity of accretionary growth which often conforms well to logarithmic spiral coiling. The study of evolutionary changes occurring in mollusc lineages relies nearly exclusively on the interpretation of shell morphologies. Important taxonomic features of molluscs include the shape of the aperture, the degree of coiling of the shell tube, the ornamentation (ribs, tubercles, spines, keels) and growth features (growth halts, constrictions, varices). The evolution of the molluscan shell is characterized by frequent convergences in form and ornamentation. As a consequence, the recognition of transformation of one shape into another crucially depends on the knowledge of how these shell shapes are generated. The comparison between different clades of molluscs can be informative with regards to the basic rules of accretionary growth. In particular, it has been pointed out that common rules of accretionary growth could underlie the morphogenesis of the shell and its evolution in ammonoids and gastropods. Evidences come from the comparison of intraspecific patterns of covariation between shell characters, from the examination of growth changes occurring at maturity and from the analysis of teratological shells with malformations caused by injuries or change in living conditions in both clades. In some highly variable ammonoids species, it has been shown that simple growth rules could underlie the evolutionary recurrent covariation of aperture shape, degree of coiling and intensity of the ornamentation (Buckman's law of covariation). Similarly, these characters covary with the spacing between growth halts during the ontogeny of some ammonoids species. A central objective of this thesis is to investigate what kinds of generic rules could produce the patterns of variation of molluscan shell shape. In a first part, it is discussed how generic models can inform us about the generation and evolution of structures of particular size and shape. In a second part, a null hypothesis model of shell growth is proposed. The intricate relationships between growth rate and allometry are described. The kind of morphological variation expected given these basic growth rules is compared to experimental evidence in developmentally plastic shells of intertidal gastropods. A population of recent gastropods (Hexaplex trunculus, Muricidae), originated from a single egg mass and bred in laboratory for about a year and a half is used to describe the ontogenetic patterns of covariation between shell characters and the dynamics of growth. This study highlights a covariation between growth rhythm (frequency and amplitude of pulses of growth), growth halts spacing, aperture allometry and intensity of ornamentation. In particular, variation in growth rhythm is regarded as critical in generating the observed covariation between growth halts spacing and ornamentation. A simple growth model is proposed to account for the integration of the covariation of these shell characters. Some recurrent patterns of variation in ammonoids species could result from similar rules tied to basic constraints of accretionary growth. The theoretical and empirical framework developed here can assist in formulating and testing new hypotheses of growth of molluscan shells. It paves the way toward the development of data-driven mathematical models which could facilitate the comparison of theoretical and empirical data in the future, and perhaps helps interpreting them in a developmental, ecological or evolutionary context. More generally, this dissertation argues that the time parameter is mandatory to the study of allometry, if one seeks to understand the relationships between size and shape and how they vary in populations.