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      Integrated phenotypes: understanding trait covariation in plants and animals

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          Abstract

          Integration and modularity refer to the patterns and processes of trait interaction and independence. Both terms have complex histories with respect to both conceptualization and quantification, resulting in a plethora of integration indices in use. We review briefly the divergent definitions, uses and measures of integration and modularity and make conceptual links to allometry. We also discuss how integration and modularity might evolve. Although integration is generally thought to be generated and maintained by correlational selection, theoretical considerations suggest the relationship is not straightforward. We caution here against uncontrolled comparisons of indices across studies. In the absence of controls for trait number, dimensionality, homology, development and function, it is difficult, or even impossible, to compare integration indices across organisms or traits. We suggest that care be invested in relating measurement to underlying theory or hypotheses, and that summative, theory-free descriptors of integration generally be avoided. The papers that follow in this Theme Issue illustrate the diversity of approaches to studying integration and modularity, highlighting strengths and pitfalls that await researchers investigating integration in plants and animals.

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          The frailty of adaptive hypotheses for the origins of organismal complexity.

          M. Lynch (2007)
          The vast majority of biologists engaged in evolutionary studies interpret virtually every aspect of biodiversity in adaptive terms. This narrow view of evolution has become untenable in light of recent observations from genomic sequencing and population-genetic theory. Numerous aspects of genomic architecture, gene structure, and developmental pathways are difficult to explain without invoking the nonadaptive forces of genetic drift and mutation. In addition, emergent biological features such as complexity, modularity, and evolvability, all of which are current targets of considerable speculation, may be nothing more than indirect by-products of processes operating at lower levels of organization. These issues are examined in the context of the view that the origins of many aspects of biological diversity, from gene-structural embellishments to novelties at the phenotypic level, have roots in nonadaptive processes, with the population-genetic environment imposing strong directionality on the paths that are open to evolutionary exploitation.
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            Perspective: Evolution and detection of genetic robustness.

            Robustness is the invariance of phenotypes in the face of perturbation. The robustness of phenotypes appears at various levels of biological organization, including gene expression, protein folding, metabolic flux, physiological homeostasis, development, and even organismal fitness. The mechanisms underlying robustness are diverse, ranging from thermodynamic stability at the RNA and protein level to behavior at the organismal level. Phenotypes can be robust either against heritable perturbations (e.g., mutations) or nonheritable perturbations (e.g., the weather). Here we primarily focus on the first kind of robustness--genetic robustness--and survey three growing avenues of research: (1) measuring genetic robustness in nature and in the laboratory; (2) understanding the evolution of genetic robustness: and (3) exploring the implications of genetic robustness for future evolution.
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              Heterochrony and allometry: the analysis of evolutionary change in ontogeny.

              The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos. Trans. R. Soc. Lond., B, Biol. Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                19 August 2014
                19 August 2014
                : 369
                : 1649 , Theme Issue ‘Phenotypic integration and modularity in plants and animals’ compiled and edited by W. Scott Armbruster
                : 20130245
                Affiliations
                [1 ]School of Biological Sciences, University of Portsmouth , Portsmouth PO12DY, UK
                [2 ]Institute of Arctic Biology, University of Alaska , Fairbanks, AK 99775, USA
                [3 ]Department of Biology, Norwegian University of Science and Technology , 7491 Trondheim, Norway
                [4 ]Center for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology , 7491 Trondheim, Norway
                [5 ]Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo , PO Box 1066, 0316 Oslo, Norway
                Author notes
                Article
                rstb20130245
                10.1098/rstb.2013.0245
                4084533
                25002693
                125af511-8121-46c7-9b71-df79db96c42c

                © 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited.

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                August 19, 2014

                Philosophy of science
                integration,modularity,variation,phenotype
                Philosophy of science
                integration, modularity, variation, phenotype

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