by Gunther J. Eble


Phenotypic integration is a central aspect of macroevolution. It is also an important concept in macroevolutionary theory. A number of empirical research questions and theoretical debates concerning evolution at and above the species level revolve around the issue of differential phenotypic integration through time. However, macroevolutionary studies in general and evolutionary paleobiology in particular have often conceptualized and documented phenotypic integration in ways that are not always comparable with standard,
quantitative-genetic microevolutionary accounts. Thus, subjects such as evolutionary radiations, constraints, morphospace structure and occupation, disparity, allometry, heterochrony and heterotopy, the origin and proliferation of novelties, and clade dynamics, to
name but a few, have been interpreted in terms of phenotypic integration (e.g., Valentine and Campbell 1975; Alberch et al. 1979 ; Maynard Smith et al. 1985; Gould 1989a,b ; Jablonski and Bottjer 1990 ; Erwin 1993 ; Zelditch and Fink 1996 ; Foote 1997 ; McGhee 1999), but with methodological protocols and theoretical motivations often distinct from those of microevolutionary research.

By extension, appreciating the status of phenotypic integration in macroevolution and its relationship with various genetic, developmental, and ecological approaches may help dissolve residual tensions between macroevolutionists and microevolutionists
(notwithstanding the fact that some scholars may belong to both communities without apparent loss of sanity!). The essential tension has concerned the issue of reducibility. It is bound to disappear, though, upon recognition that macroevolution is not completely reducible to microevolution because of differences in scale, in the hierarchical manifestation of evolutionary processes, in the extent and sources of contingency and constraint, and in the nature of the focal biological entities (Gould 1982, 2002; Eldredge 1989; Williams 1992; Erwin 2000; Jablonski 2000). None of these justifications for a relative autonomy of macroevolution are necessarily contentious nowadays, as macroevolutionary research has been rendered more rigorous conceptually, empirically, and theoretically, with operational definitions and methodologically sophisticated data collection, analysis, and modeling routinely guiding statistically testable inferences about large-scale evolutionary patterns and processes (Schopf 1972 ; Raup and Jablonski 1986 ; Gilinsky and Signor 1991; Erwin and Anstey 1995; Jablonski et al. 1996; Foote 1997; McKinney and Drake 1998 ; Eble 2000a, 2002a; Jablonski 2000; Jackson et al. 2001; Gould 2002). Macroevolution and microevolution are at times factually and theoretically distinct, but material irreducibility is only partial, and complete decouplement is logically impossible, because actual organisms must figure in both domains. There is no fundamental incompatibility between macroevolution and microevolution in a general evolutionary theory, if such theory incorporates biological hierarchies as matters of fact or at least as heuristic representations.

Cross-hierarchical organization and dynamics are complex, but not intractable (Simon 1962 ; Lewontin 1970; Weiss 1971; Eldredge 1985; Vrba and Gould 1986 ; Vrba 1989 ; Eble 1999a; McShea 2001; Gould 2002), and the existence of biological hierarchies per se does not necessarily demand level-specific theories of process (e.g., Williams 1992; Maynard Smith and Szathmáry 1995). At issue, then, is precisely which phenomena, explanations, and theoretical constructs associated with macroevolution are equivalent to those in the microevolutionary realm, which are only partially equivalent, and which – if any – are incommensurable. The study of phenotypic integration is of special relevance in this regard, since the phenotype figures in empirical and theoretical research in population biology, in systematics, in evolutionary developmental biology, and in paleobiology. Clarifying how phenotypic integration is manifested and studied in macroevolution, and understanding the nature of macroevolutionary phenotypic integration, may help in moving beyond the perhaps overly modular multidisciplinarity of current integration studies and towards a more unifying interdisciplinarity (Zelditch 1996 ; Schlichting and Pigliucci 1998). This in turn may open the way for a more synthetic appreciation of the role of the phenotype in evolutionary theory at large.

In this contribution, I will examine this state of affairs and discuss macroevolutionary issues that have been or could be analyzed in the context of phenotypic integration, either explicitly or implicitly. In doing so, I will suggest that research protocols for studying the
macroevolution of phenotypic integration are appropriate for certain questions but must be further refined to tackle a wider array of macroevolutionary problems and to allow new models to be advanced, and that certain conceptual and analytical approaches in
macroevolution may prove useful, or at least illuminating, in microevolution as well. The intent, as unavoidable in a subject still in need of a synthesis, is not to be exhaustive or prescriptive, but to simply highlight the unique contexts of macroevolutionary phenotypic integration, and the phenomenology of causes it implies. This can be viewed as a step towards developing a more solid account of the meaning of pattern and process in macroevolution, in a manner that is at the same time compatible with and enriching of
microevolutionary theory.