The Pattern of Variation in Centipede Segment Number as an Example of Developmental Constraint in Evolution

Ecology Centre, University of Sunderland, Sunderland, SR1 3SD, U.K.
Journal of Theoretical Biology (Impact Factor: 2.12). 10/1999; 200(2):183-91. DOI: 10.1006/jtbi.1999.0986
Source: PubMed


The range of animal morphologies observed in nature is partly determined by natural selection. However, there is no agreement yet regarding whether it is also partly determined by developmental constraint. Testing for the effects of constraint has been difficult due to the lack of both an appropriate null model and a sufficiently simple system capable of yielding unambiguous results regarding the model's plausibility. Here we examine the case of variation in segment number in geophilomorph centipedes. Curiously, while this ranges between 29 and 191, there are no species in which an even number of segments is observed, in contrast to about 1000 species with odd numbers of segments. It seems unlikely that this distribution of character values is determined by selection alone. Using an approach based on Bayesian inference, we attempt to quantify the probability of obtaining the observed distribution of values given a null model in which developmental constraint is absent. Since this probability is in the region of 10(-20), we conclude that constraint must be involved. We discuss various implications of this conclusion, and comment on the unexpected absence of neoteny and progenesis in centipede evolution. Copyright 1999 Academic Press.

Download full-text


Available from: Wallace Arthur, May 29, 2014
  • Source
    • "Further evidence for this hypothesis comes from centipedes where the number of trunk segments is always odd (reviewed in [72,73]). This shows that there may be a genetic constraint that does not allow for the formation of an even number of trunk segments in centipedes [74]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning. Expression analysis of pair rule gene orthologs in the blastoderm of the pill millipede Glomeris marginata (Myriapoda: Diplopoda) suggests that these genes are generally involved in segmenting the anterior embryo. We find that the Glomeris pairberry-1 ( pby-1) gene is expressed in a pair rule pattern that is also found in insects and a chelicerate, the mite Tetraynchus urticae. Other Glomeris pair rule gene orthologs are expressed in double segment wide domains in the blastoderm, which at subsequent stages split into two stripes in adjacent segments. The expression patterns of the millipede pair rule gene orthologs resemble pair rule patterning in Drosophila and other insects, and thus represent evidence for the presence of an ancestral pair rule-like mechanism in myriapods. We discuss the possibilities that blastoderm patterning may be conserved in long-germ and short-germ arthropods, and that a posterior double segmental mechanism may be present in short-germ arthropods.
    BMC Developmental Biology 05/2012; 12(1):15. DOI:10.1186/1471-213X-12-15 · 2.67 Impact Factor
  • Source
    • "The importance of the former can be examined in several ways. The observation that a particular phenotype is never produced either within or among species—such as an even number of legs in adult geophilomorph centipedes (Arthur and Farrow 1999)—suggests that the lack of species bearing that phenotype is a result of an intrinsic constraint, rather than selective disadvantage (the dichotomy between selection and constraint becomes fuzzy when one considers the possibility that variation arises during development, but the embryo cannot function and dies. Is this a developmental constraint on the production of variation or evidence of selection on an inferior phenotype? "
    [Show abstract] [Hide abstract]
    ABSTRACT: Convergent evolution of similar phenotypic features in similar environmental contexts has long been taken as evidence of adaptation. Nonetheless, recent conceptual and empirical developments in many fields have led to a proliferation of ideas about the relationship between convergence and adaptation. Despite criticism from some systematically minded biologists, I reaffirm that convergence in taxa occupying similar selective environments often is the result of natural selection. However, convergent evolution of a trait in a particular environment can occur for reasons other than selection on that trait in that environment, and species can respond to similar selective pressures by evolving nonconvergent adaptations. For these reasons, studies of convergence should be coupled with other methods-such as direct measurements of selection or investigations of the functional correlates of trait evolution-to test hypotheses of adaptation. The independent acquisition of similar phenotypes by the same genetic or developmental pathway has been suggested as evidence of constraints on adaptation, a view widely repeated as genomic studies have documented phenotypic convergence resulting from change in the same genes, sometimes even by the same mutation. Contrary to some claims, convergence by changes in the same genes is not necessarily evidence of constraint, but rather suggests hypotheses that can test the relative roles of constraint and selection in directing phenotypic evolution.
    Evolution 07/2011; 65(7):1827-40. DOI:10.1111/j.1558-5646.2011.01289.x · 4.61 Impact Factor
  • Source
    • "In the debates following this famous critique, special attention was given to constraints that are inherent to development (Pigliucci and Kaplan 2000), because the impossibility of producing complex phenotypes may also be the reason for observed biological features (universal constraints as defined by Maynard-Smith et al. 1985), and developmental constraints may be seen as a prime phenotypic filter before natural selection (Arthur 2001, 2002). This debate has been strongly theoretical (Resnik 1995) and so far little empirical investigation has been produced in favor of developmental constraints (e.g., Gould 1989; Vogl and Rienesl 1991; Arthur and Farrow 1999). On the other hand, some studies investigating this question favored adaptive explanations over historical effects (Janson 1992; Travisano et al. 1995; Miller et al. 2006). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Developmental constraints have been proposed to interfere with natural selection in limiting the available set of potential adaptations. Whereas this concept has long been debated on theoretical grounds, it has been investigated empirically only in a few studies. In this article, we evaluate the importance of developmental constraints during microsporogenesis (male meiosis in plants), with an emphasis on phylogenetic patterns in Asparagales. Different developmental constraints were tested by character reshuffling or by simulated distributions. Among the different characteristics of microsporogenesis, only cell wall formation appeared as constrained. We show that constraints may also result from biases in the correlated occurrence of developmental steps (e.g., lack of successive cytokinesis when wall formation is centripetal). We document such biases and their potential outcomes, notably the establishment of intermediate stages, which allow development to bypass such constraints. These insights are discussed with regard to potential selection on pollen morphology.
    Evolution & Development 09/2007; 9(5):460-71. DOI:10.1111/j.1525-142X.2007.00183.x · 2.72 Impact Factor
Show more