Molecular Evolution and Adaptive Radiation - Review

Ecology, Jan, 1999 by Patrick Foley

Givnish, Thomas J., and Kenneth J. Sytsma, editors. 1997. Cambridge University Press, New York. xvii 621 p. $105.00, ISBN: 0-521-57329-7.

An old instructional film on molluscan diversity by Ralph Buchsbaum ends with the congratulatory statement that the Molluscs provide a good example of the principles of adaptive radiation. But what are those principles? And if Darwin was correct about adaptive evolution, don't all branches of the phylogenetic tree of life provide good examples of adaptive evolution? In the first chapter of Molecular evolution and adaptive radiation (MEAR), Givnish outlines alternatives to adaptive radiation (non-adaptive, developmental, sexual, and coevolutionary radiations) and demonstrates how the study of adaptive radiation provides insight into adaptation, speciation, biogeography, and historical ecology.

Evolutionary ecologists have long argued about the rate of niche specialization, the pace of co-evolutionary races, the sequence of community assemblage, host acquisition, and pollinator co-option. Until recently, such speculations risked circular reasoning. Phylogeny based on morphology (often plainly adaptive) is phylogeny based partly on homoplasy, i.e., convergent and parallel evolution. Molecular systematics points out a path away from circularity. DNA sequences (hopefully unlinked to the genes governing an adaptive radiation) can give us the phylogeny. We can, in principle, reconstruct the historical sequence of adaptive trait acquisition throughout this independently constructed phylogeny. This is the Darwinian program at its most elegant.

There are some problems left. Givnish and Sytsma, in the second chapter of MEAR, attempt to estimate the rate of homoplasy in molecular versus morphological traits. While they favor molecular phylogenies as less homoplasious, their study is not unequivocal since, for example, base-pairs and amino acids revert readily to earlier states, the direction of evolution is often hard to judge, and size confusions are common in fragment length polymorphism studies. Moreover, there remain controversies over the statistical technicalities of cladogram construction, for example the utility of maximum likelihood over maximum parsimony. But these problems are largely solvable, given enough data and a little tolerance. More problematic is the regrettable tendency of clades to speciate in bursts. This makes for short, confidence-eroding branches in otherwise well-resolved phylogenetic trees. The classic examples are the Cambrian explosion of animal phyla and the K/T explosion of mammal orders. Several chapters of MEAR confirm this pattern that G. G. Simpson recognized as due to the occupation of new "adaptive zones."

Nineteen of the 21 chapters of MEAR are case studies for particular clades, ranging from genus to class in taxonomic extent. Flowering plants are well represented with chapters on Hawaiian silverswords and Alsinoideae, columbines, Pontederiaceae, Guyana Shield Brocchinia, Macaronesian Argyranthemum, and two groups of orchids (the Oncidiine twig epiphytes and the terrestrial Platanthera). The animal lineages include cicindelid beetles, Hawaiian Drosophila, North American Daphnia, Caribbean Anolis lizards, African cichlids, British Columbian sticklebacks and other lake fishes, Old World fruitbats, New World monkeys, post-Gondwanaland marsupials, and post-paleozoic echinoids. The usual chapter format is to lay out the molecule-based phylogeny and then to discuss the morphological, adaptive evolution in an ecological context. In evolution as in ecology, everything is a special case, so chapter conclusions should not be taken too universally. Nonetheless there are some striking conclusions.

Sympatric speciation may be more common in lake fish than believed by Ernst Mayr (Reinthal and Meyer; Taylor et al.; and McCune). Evolution repeats itself (at least for lizards on four Caribbean islands and loosely for marupials in Australia and South America), contra Stephen Gould (Jackman et al.; Springer et al.). Molecular evidence often contradicts orchid flower morphology-based phylogeny (Hapeman and Inoue; and Chase and Palmer) and homoplasy abounds in the morphology of adaptive radiation (many chapters of the book). The taxon-cycle model of E. O. Wilson is not well supported by American tiger beetles, and it may be unrestable by phylogenetic analysis (Vogler and Goldstein). Within a single unspeciose bromeliad genus, more adaptive radiation in nutrient capture (tanks, trichomes, and such) has occurred than in any other plant genus; adaptation is not here the accidental product of massive speciation and species selection as Gould, Stanley, and others would have it (Givnish et al.). Endemic Hawaiian drosophilids are indeed monophyletic with stepwise adaptive shifts in diet from fungus to leaves to stem to bark and finally tree fluxes (Kambysellis and Craddock).

The shift to sexual dimorphism in xeric Alsinoideae is rarer (it has happened once or twice) than the reversion to hermaphroditism in these Caryophyllaceae (Sakai et al.). While the silversword ancestor arose from western North American tarweeds about 15 million years ago, the present alliance of 28 Hawaiian species has evolved into its diversity of forms and habitats in the last 6 million years (Baldwin). Daphnia however had its burst of diversification in the Mid-Mesozoic and has shown little innovation since (Colbourne et al.). The spurs of columbines appear to be a key innovation (contra Craycraft) that permitted their diversification even in the widespread (and thus exposed to competitors) genus Aquilegia (Hodges). There is of course more in this book than a quick review can cover.