Evolutionary Constraints

by

Thomas F. Hansen

• LAST REVIEWED: 15 January 2015
• LAST MODIFIED: 15 January 2015
• DOI: 10.1093/obo/9780199941728-0061

Introduction

Evolutionary constraints are restrictions, limitations, or biases on the course or outcome of adaptive evolution. The term usually describes factors that limit or channel the action of natural selection. It is not equivalent to evolutionary stasis (absence of change) or even to factors that cause stasis. Evolutionary stasis may be caused by stabilizing selection, but stabilizing selection caused by the external environment is not usually considered a constraint. In a general sense all evolution is constrained. There are no Darwinian demons, immortal organisms that can reproduce infinitely fast, and the concept of constraint is most useful in relation to specific traits, selective agents or ecological contexts. Constraints occur when a trait is precluded from reaching, shifted away from, or slowed down in its approach to a (defined) selective optimum. Interest in the interplay between selection and constraints goes back to Darwin, and specifically to his concept of correlation of growth, which he used to explain how traits may change as side effects of selection on other traits. The fundamental idea is that selection acts on variation so that the structure and availability of variation may constrain what selection can do. Constraint thinking also has links to orthogenesis, the notion that evolution is driven in particular directions by some internal lineage-specific force rather than by external selection caused by interactions with the environment. Orthogenesis was rejected during the modern synthesis due to a lack of plausible mechanism, accumulating evidence for local adaptations, and an emerging understanding of macroevolution as a messy historical process rather than a rectilinear march toward perfection. The modern synthesis saw increasing emphasis on functional explanations based on external natural selection while structural explanations based on development became marginalized. This was influenced first by the realization that selection can act efficiently on minute differences, and later by the empirical findings of large amounts of genetic variation both on molecular and organismal levels. Hence, mainstream evolutionary biology increasingly took it as given that the necessary variation for selection to act was available. After a nadir in the 60s, a structuralist perspective with an emphasis on developmental constraints started to reemerge. This was manifest first in the revival of concepts such as heterochrony and allometry, which may be seen as specific constraints on evolution, and later in the emerging field of evolutionary developmental biology, or evodevo, where the study of developmental constraints is central. An important element in the modern treatment of constraints is that constraints are not just seen as limitations and explanations of last resort, but are also assigned positive explanatory roles based on channeling variation in directions that may facilitate and explain adaptation.

Overview

Few concepts in biology are as manifold and lacking in consensus as that of constraints. The state of the terminology is well summarized by the title of Antonovics and van Tienderen 1991, “Ontoecogenophyloconstraints? The Chaos of Constraint Terminology.” A good entry point to this chaos is Arnold 1992, a review in which types of constraints are organized in an interacting hierarchy. On the top level are genetic constraints, which are reasonably well operationalized in terms of standing genetic variation. Levels of genetic variation may limit evolution if they are absent or too low, or if variation in different traits are bound up with each other by genetic correlations. The underlying cause of genetic constraints is developmental constraints, which control the input of new genetic variation through mutation, and thus determine genetic constraints in interaction with selection. Selective and functional constraints refer to effects of selection on other traits or for other functions than the focal adaptation, and thus explain how genetic correlations constrain evolution. They also help explain patterns of genetic variation that stem from fundamental trade-offs and physical limitations that no biological system can circumvent. Phylogenetic and historical constraints are orthogonal to this scheme. Here the emphasis is on the role of ancestry in determining the subsequent course of evolution. This is both because the species may inherit particular traits or developmental systems that constrain the possible variation that forms the basis for new adaptations, and because the ancestral position in a complex adaptive landscape can influence which local adaptive peak is eventually reached. Schwenk 1995 and Richardson and Chipman 2003 provide other classifications of constraint terminology. Futuyma 2010 is a recent review of explanations for stasis in evolution showing that maladaptation is common and that there is room for constraints as an explanatory factor alongside adaptation. Gould 2002 and Amundson 2005 provide historical overviews of structuralist positions in evolutionary biology in which developmental and historical constraint concepts are central.

• Amundson, R. 2005. The changing role of the embryo in evolutionary thought. Cambridge Studies in Philosophy and Biology. Cambridge, UK, and New York: Cambridge Univ. Press.

  DOI: 10.1017/CBO9781139164856

  A historical overview of structuralist thinking in evolution and of the relationship between development and evolution.

• Antonovics, J., and P. H. van Tienderen. 1991. Ontoecogenophyloconstraints? The chaos of constraint terminology. Trends in Ecology & Evolution 6:166–168.

  DOI: 10.1016/0169-5347(91)90059-7

  A review of constraint terminology with an immortal title.

• Arnold, S. J. 1992. Constraints on phenotypic evolution. American Naturalist 140:S85–S107.

  An influential review of types of constraint and their relationships.

• Futuyma, D. J. 2010. Evolutionary constraint and ecological consequences. Evolution 64:1865–1884.

  DOI: 10.1111/j.1558-5646.2010.00960.x

  A recent review of mechanisms for evolutionary stasis with discussions of the role of constraint.

• Gould, S. J. 2002. The structure of evolutionary theory. Cambridge, MA: Belknap.

  Gould’s magnum opus with extensive discussions of developmental and historical constraints, and much material on the history of evolutionary biology.

• Richardson, M. K., and A. D. Chipman. 2003. Developmental constraints in a comparative framework: A test case using variation in phalanx number during amniote evolution. Journal of Experimental Biology Part B: Molecular and Developmental Evolution 296 B:8–22.

  A classification of constraint terminology emphasizing the fundamental distinction between generative and selective constraints. Discuss how to test constraint in a comparative setting through the example of phalanx numbers in amniotes.

• Schwenk, K. 1995. A utilitarian approach to evolutionary constraint. Zoology 98:251–262.

  A general review of evolutionary constraints.