The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

Abstract

Variation is the raw material for natural selection, but the factors shaping variation are still poorly understood. Genetic and developmental interactions can direct variation, but there has been little synthesis of these effects with the extrinsic factors that can shape biodiversity over large scales. The study of phenotypic integration and modularity has the capacity to unify these aspects of evolutionary study by estimating genetic and developmental interactions through the quantitative analysis of morphology, allowing for combined assessment of intrinsic and extrinsic effects. Data from the fossil record in particular are central to our understanding of phenotypic integration and modularity because they provide the only information on deep-time developmental and evolutionary dynamics, including trends in trait relationships and their role in shaping organismal diversity. Here, we demonstrate the important perspective on phenotypic integration provided by the fossil record with a study of Smilodon fatalis (saber-toothed cats) and Canis dirus (dire wolves). We quantified temporal trends in size, variance, phenotypic integration, and direct developmental integration (fluctuating asymmetry) through 27,000 y of Late Pleistocene climate change. Both S. fatalis and C. dirus showed a gradual decrease in magnitude of phenotypic integration and an increase in variance and the correlation between fluctuating asymmetry and overall integration through time, suggesting that developmental integration mediated morphological response to environmental change in the later populations of these species. These results are consistent with experimental studies and represent, to our knowledge, the first deep-time validation of the importance of developmental integration in stabilizing morphological evolution through periods of environmental change.phenotypic integration | modularity | macroevolution | carnivorans |

Developmental bias in the fossil record

“…Due to the internal architecture of developmental systems, which generates integrated modules (Goswami, Binder, Meachen, & O'Keefe, 2015;Schlichting, 1989;Wagner & Zhang, 2011), random genetic mutations may still lead to coordinated phenotypic responses (Jablonski, 2017;Moczek et al, 2011;Uller et al, 2018;West-Eberhard, 2003). For this reason, the effects of the previously cryptic genetic variation may, in fact, cause directed phenotypic change, biased towards functionally integrated phenotypes (Gerhart & Kirschner, 2007;Masel, 2006;Wagner, 2011;Watson & Szathmáry, 2016;Watson, Wagner, Pavlicev, Weinreich, & Mills, 2014).…”

Developmental bias, macroevolution, and the fossil record

“…Comparative developmental or variational analyses of clades that conform to the relinkage model, versus those that do not, coupled with functional analyses of the traits associated with such shifts, are much needed. This might be the expectation if modularity tends to increase and phenotypic integration tends to decrease over clade histories, as suggested by Goswami et al (2014). For example, the diversification of beaks in the early Cenozoic radiation of modern birds might be viewed in this way (Uller et al, 2018).…”

“…For a given structure or region of the body, stronger developmental integration and weakly defined modules are generally held to impede and channel evolutionary change, whereas weaker integration and more sharply defined modules appear to afford greater freedom to evolving lineages, in the sense that among-module changes are facilitated (while within-module ones will be hindered; see Goswami, Binder, Meachen, & O'Keefe, 2015;Goswami, Smaers, Soligo, & Polly, 2014;Porto, Shirai, de Oliveira, & Marroig, 2013;Sears, 2014;Uller et al, 2018;, who view allometry as a special case of developmental integration). It is often treated as the converse of integration, although some care is needed in that an organism can have weak integration but lack discrete modules.…”

“…F I G U R E 1 (a) Measurement of evolutionary change and its correspondence to within-population variation. Smith and Kroh (2011), © The Trustees of the Natural History Museum, London, licensed under the Open Government Licence [Color figure can be viewed at wileyonlinelibrary.com] Empirically, strong integration shows the expected association with both low disparity and low evolutionary rates in the avian skull, but only with low disparity in the mammalian skull (Bright, Marugán-Lobón, Cobb, & Rayfield, 2016;Goswami et al, 2014;). After Hunt (2007), who found that evolutionary changes in the fossil ostracode Poseidonamicus were significantly aligned with P max in ancestor-descendent transitions.…”

Morphological integration in human skull and its possible role in etiogenesis of neuropsychiatric disorders: Deciphering the link between evolution, development and disease

“…Plausibly, these variations accumulated in the long course of evolution (33)(34)(35), through assimilation of co-variances (34,35) and epigenetic changes (36) in the gross and genetic structure of a population respectively, implied morphological integration (34,37). The inclusion of variations in the skull components in the course of evolution might have subjected a population to acquire and propagate multiple errors at molecular level (3) and to express these as aberrant genotypes and phenotypes (38), setting basis for etiogenesis of certain neuropsychiatric disorders (10,12,18,7).…”