Is Modularity Necessary for Evolvability? Remarks on the Relationship between Pleiotropy and Evolvability

Department of Biological Science, Florida State University, Tallahassee, FL 32306, USA.
Biosystems (Impact Factor: 1.55). 06/2003; 69(2-3):83-94.
Source: PubMed


Evolvability is the ability to respond to a selective challenge. This requires the capacity to produce the right kind of variation for selection to act upon. To understand evolvability we therefore need to understand the variational properties of biological organisms. Modularity is a variational property, which has been linked to evolvability. If different characters are able to vary independently, selection will be able to optimize each character separately without interference. But although modularity seems like a good design principle for an evolvable organism, it does not therefore follow that it is the only design that can achieve evolvability. In this essay I analyze the effects of modularity and, more generally, pleiotropy on evolvability. Although, pleiotropy causes interference between the adaptation of different characters, it also increases the variational potential of those characters. The most evolvable genetic architectures may often be those with an intermediate level of integration among characters, and in particular those where pleiotropic effects are variable and able to compensate for each other's constraints.

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    • "From an evolutionary perspective, indeed, if different characters are able to vary independently, selection will be able to optimize each character separately. For this reason , the concept of modularity has been linked to evolvability , the ability of a biological unit to respond to a selective challenge (Hansen 2003). One of the most intensively studied traits to investigate the effect of Robertsonian fusions in producing intra-and interpopulations phenotypic differences is the mouse mandible (Corti and Rohlf 2001;Sans-Fuentes et al. 2009;Mu~ noz-Mu~ noz et al. 2011;Martinez-Vargas et al. 2014). "
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    • "A property of living systems that is well suited to explain the origin of morphological disparity is their modular organization (Wagner 1996; Hansen 2003; Wagner et al. 2007; Pavlicev and Hansen 2011). Organisms are hypothesized to be constructed from distinct sub-units termed modules that are highly integrated internally and behave quasi-independently during ontogeny and evolution (Wagner 1996; von Dassow and Munro 1999; Hansen et al. 2003; Klingenberg et al. 2003; Wagner et al. 2007; Kuratani 2009). Modularity is tightly linked to the concept of morphological integration, which postulates that functionally or developmentally related traits should form highly cohesive morphological units (Olson and Miller 1958; Cheverud 1982; Zelditch 1987; Cheverud 1996; Chernoff and Magwene 1999). "
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    ABSTRACT: Actinopterygians demonstrate high levels of morphological disparity, especially in the variation of fin positions, sizes and shapes. One hypothesis to explain the diversity of fin morphologies is that it is facilitated by a modular organization. According to this hypothesis, fin modules would be quasi-independent during ontogeny or evolution, facilitating their evolvability. We investigated variational modularity of fins in two cyprinid species, the zebrafish (Danio rerio) and the Northern redbelly dace (Chrosomus eos), to determine which subsets of fins are quasi-independent and which are most highly integrated in positioning. Hypotheses of modularity were evaluated using a combination of methods suitable for analyses of landmarks. The hypothesis that the dorsal and anal fins belong to a posterior trunk and tail module is strongly supported, a finding that can be explained by the use of subcarangiform locomotion in these two species. There is also some support for the hypothesis that the paired fins and head region each constitute variational modules. The support for fin variational modules is weaker than expected considering the wealth of developmental evidence supporting fin modularity. This might be related to a dissociation of the fin positioning modules during actinopterygian evolution, a process that had already been suggested for the dorsal and anal fins. Alternatively, the fin modules inferred from developmental data might not directly translate into variational modules: variational modules can incorporate the signals from numerous partially overlapping developmental processes so that one to one correspondence between developmental and variational modules is not always expected.
    No preview · Article · Jun 2015 · Evolutionary Biology
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    • "phenotype map (e.g. Mezey et al. 2000; Cheverud 2001; Hansen 2003; Pigliucci 2010) has several components. To a large extent, difficulties in this area derive from the arbitrary way we dissect the phenotype into individual characters, in the usually vain hope to find a simple one-to-one correspondence between genes and characters. "
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    ABSTRACT: Evolutionary developmental biology (evo-devo) is a rapidly growing discipline whose ambition is to address questions that are of relevance to both evolutionary biology and developmental biology. This field has been increasingly progressing as a new and independent comparative science. However, we argue that evo-devo's comparative approach is challenged by several metaphysical, methodological and socio-disciplinary issues related to the foundation of heuristic functions of model organisms and the possible criteria to be adopted for their selection. In addition, new tools have to be developed to deal with newly chosen model organisms. Therefore, we present a modelling framework suitable to integrate data on individual variation into evo-devo studies on new model organisms and thus to compensate for current idealization practices deliberately suppressing variation.
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