# Understanding macroevolution through the origin of higher taxa

Simpson, C. 2016. Understanding macroevolution through the origin of higher taxa. Ecology, 97: 3246–3248. doi:10.1002/ecy.1550 link

Review of: Understanding macroevolution through the origin of higher taxa Kemp, T. S. 2015. The origin of higher taxa: palaeobiological, developmental, and ecological perspectives. The University of Chicago Press, Chicago, Illinois. 320 p. $120.00 (cloth), ISBN: 978-0-2263-3581-0; 320 p.$49.00 (paper), ISBN: 978-0-2263-3595-7; 320 p. \$39.00 (e-book), ISBN: 979-0-2263-3600-8.

Key words: speciation; ontology; epistemology; phenotypic traits; developmental evolution; macroevolutionary lags; character identity networks.

Higher taxa originate often enough that the major phases of the geologic timescale can be quantified by their turnover. But the origination of new higher taxa is rare relative to the origin of new species. Only a subset of speciation events that are associated the origin of one or more novel traits and with the occupation of new ecologies that lead to new higher taxa. This confluence of developmental and ecological novelty leads to innovation and the proliferation of these traits that makes it important and interesting to study the origin of higher taxa.

Tom Kemp (Oxford University) in his new book The origin of higher taxa makes an argument for just how important it is for us to understand their origin. In this book, Kemp summarizes and synthesizes what we currently know about the origin of higher taxa. Because ecological, phenotypic, and developmental attributes of organisms all change during the origin of higher taxa, Kemp pulls evidence from the fields of ecology, developmental biology, and paleontology to buttress his arguments that there really is an interesting scientific question here.

And the origin of higher taxa really is interesting, even if the interesting questions are constantly nagged by the possibility that higher taxa may not be real. For some, the reality of higher taxa is important, because if they lack realness, then why bother studying them? I don’t share that cynical view, but it is commonly held. For some, higher taxa are arbitrary products of our work to classify organisms, so to study their origins is nothing more than studying the act of classification rather than the evolution of organisms—more an act of philosophy than an act of science. But that cynical attitude misses the point. The origins of higher taxa are inherently interesting because, as Kemp points out, the confluence of changes that occur there represent discontinuities in the macroevolution of lineages. The confluence of changes associated with the origins of higher taxa are observed phenomena. How and why that confluence occurs is an interesting question, even if higher taxa that arise out of that confluence are not themselves real.

The struggle between ontology and epistemology is a theme throughout the book. Each line of evidence comes from a scientific discipline that provides insights but never the whole picture. Kemp spends a lot of time delineating the limits of each possible view on the origins of higher taxa. The paleontological evidence is particularly tricky because the fossil record samples past life in non-random ways. The hope that the fossil record will preserve ancestral forms and allow the easy study of higher taxa is dashed by the fact that ancestors are somewhat rare. Nevertheless, the fossil record is critical because it gives us real examples. It shows that the origins of higher taxa share some similarities and also show some important differences. In some groups, such as irregular echinoids (Hopkins and Smith 2015) their radiation happens close to their time of origin. Yet in other groups, such as grasses, there is a protracted lag between the origin of the group and their subsequent radiation (Strömberg 2011).

The existence of macroevolutionary lags means that the developmental, phenotypic, and ecological changes that occur during the origin of higher taxa don’t always happen together. In the evolution of grasses, the ecological opportunity for grasslands significantly postdates the origin of grasses themselves. This lag is due to complex interactions between different higher taxa (various herbivorous mammal groups and other plant groups that compete for space with grasses) and climate changes.

The structure and evolutionary potential of organisms provides the foundation of Kemp’s thoughts on the origin of higher taxa. The phenotypic traits of organisms interact with each other functionally and developmentally. Kemp argues that phenotypic traits evolve as an ensemble within populations of organisms by the correlated progression model. This is a model of developmental evolution that he contrasts with the atomistic and modular models. Each of these three models differ only in how the phenotypic traits are connected by a network of interactions. The atomistic model has few connections, the modular model has strong connections within modules and weak between. His correlated progression model hits in-between these, with all traits having a more even distribution of interactions. For Kemp, this model of developmental evolution provides the only route for the suite of phenotypic changes that occur during the origin of higher taxa. However, I’m not sure we need to restrict ourselves to a single model of developmental evolution. Recent theoretical work by Sean Rice (Rice 2004a, b, 2008) provides an alternative way of understanding developmental evolution that includes all possible interactions networks. Rice’s approach produces a phenotypic landscape that is the result of a set of variously underlying factors (genetic, developmental, and environmental), and the path of multivariate phenotypic evolution is described by the structure of that landscape.

Thinking about developmental evolution from the theoretical distance that Rice takes makes it clear that there is another aspect of developmental evolution that is important for the origins of higher taxa—phenotypic novelty. The origin of novel traits, those autapomorphies that characterize higher taxa, are a critical part of the story. Novelties are the source of the phenotypic discontinuities between higher taxa, and so understanding how they arise is critical to understand the origin of higher taxa. I am not sure how Kemp’s correlated progression model deals with novelty. Wagner (2014) provides a powerful way to think about novelty and its role in developmental evolution through the evolution of homologous traits. According to Wagner, homologues arise when recursive character identity networks (ChINs) are added into the developmental pathway that produces a phenotypic trait. The addition of novel ChINs into the development of an organism is sufficient to provide a discontinuity in overall phenotypes, because part of the phenotype did not exist prior to the origin of the ChIN.

The evolution of irregular echinoids from regular echinoids (Hopkins and Smith 2015) is good example of how complicated the origin of higher taxa can be and yet still be understood. The origin of irregular echinoids involves major shifts in development and ecology and can be seen as a large jump in morphospace. In their study, Hopkins and Smith (2015) show that the paraphyletic regular echinoids are phenotypically contained prior to the divergence of irregulars and that they remain similarly constrained after the split. Irregulars immediately show higher rates of morphological evolution as they occupy new areas of morphospace associated with feeding structures and a new ecology. This shift requires that the developmental capacity of irregulars evolve together with their ecological innovations.

Kemp’s book is a good introduction to the ontological and epistemological issues inherent in the study of the origins of higher taxa. I suspect that this is the path that will lead to a new evolutionary synthesis because it focuses our attention onto the mechanisms that produce phenotypic and ecological discontinuities. Those higher taxa that show a macroevolutionary lag between the developmental novelties at their origin and ecological innovations that proliferate when they become successful are the most promising cases for teasing apart how it all works. If ecological interactions between higher taxa are important factors in the duration of macroevolutionary lags, as Van Valen (1976) suggests, then we might have to embrace the reality and evolutionary significance of higher taxa.

Literature cited

Hopkins, M. J., and A. B. Smith. 2015. Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution. Proceedings of the National Academy of Sciences 112:3758-3763.

Rice, S. H. 2004a. Developmental associations between traits: covariance and beyond. Genetics 166:513-526.

Rice, S. H. 2004b. Evolutionary theory: mathematical and conceptual foundations. Sinauer Associates, Sunderland, Massachusetts.

Rice, S. H. 2008. Theoretical approaches to the evolution of development and genetic architecture. Annals of the New York Academy of Sciences 1133:67-86. Strömberg, C. A. 2011. Evolution of grasses and grassland ecosystems. Annual Review of Earth and Planetary Sciences 39:517-544.

Van Valen, L. 1976. Energy and evolution. Evolutionary Theory 1:179-229.

Wagner, G. P. 2014. Homology, genes, and evolutionary innovation. Princeton University Press, Princeton, New Jersey.