Indeterminate Growth: Could It Represent the Ancestral Condition?

Abstract

Although we are used to the idea that many organisms stop growing when they reach a predictable size, in many taxa, growth occurs throughout the life of an organism, a phenomenon referred to as indeterminate growth. Our comparative analysis suggests that indeterminate growth may indeed represent the ancestral condition, whereas the permanent arrest of growth may be a more derived state. Consistent with this idea, in diverse taxa, the basal branches show indeterminate growth, whereas more derived branches arrest their growth. Importantly, in some closely related taxa, the termination of growth has evolved in mechanistically distinct ways. Also, even within a single organism, different organs can differ with respect to whether they terminate their growth or not. Finally, the study of tooth development indicates that, even at the level of a single tissue, multiple determinate patterns of growth can evolve from an ancestral one that is indeterminate.

Figure 1.

Ontogenetic trajectories. (A) The ontogenetic trajectory of an organism is shown as a point moving in three dimensions: size (S), shape (σ), and age (a). (B) Linearized ontogenetic trajectories are shown as a plot of shape (σ) versus age (a). Species 2 can achieve a final shape that is different to that of species 1 either by having a different rate of shape change (2), a different time of onset of growth (2′), or a delayed offset (2′′). (C) Species 1 has determinate growth, whereas species 2 has indeterminate growth. By showing plots of shape versus age, rather than size versus age, the growth characteristics of species that differ considerably in size can be easily compared.

Figure 2.

Phylogenetic relationships of (A) insect (Giribet and Edgecombe 2012), and (B) annelid (Ferrier 2012) species. Note that the more basal branches show indeterminate growth. The asterisks indicate paraphyletic taxa.

Figure 3.

Common patterns of teeth in vertebrates. Teeth in vertebrates are variable within clades in shapes, patterns of arrangement on the jaws (or other elements), and numbers of both teeth and the rows in which they occur in adults. (A) Homodonty: all teeth in a row the same shape (many fishes, amphibians, reptiles). (B) Heterodonty: teeth different shapes in a row (e.g., the incisors, canines, and molars of many mammals). (C) Monodonty: a single row of functional teeth. (D) Diphyodonty: two sets of teeth, a juvenile dentition that is replaced by an adult set (e.g., many mammals, including humans). (E) Polyphyodonty: multiple rows of teeth (or patches) with teeth being shed and new teeth developing from adjacent loci to replace them throughout life (e.g., most fishes, amphibians, and reptiles). (F) Polystichy: multiple rows of teeth with several rows of functional teeth accumulated on the jaws (or in patches) without being serially shed (e.g., sharks). (G) Edentulous: tooth development suppressed (e.g., some frogs, birds). Note that A, B, C, and G may not involve replacement, depending on the lineage. Functional teeth are blue; replacement teeth in loci are white.