Reflections On The Evolution Of Ecological Traits

When I began studying phylogenetic systematics in the late 1970s, it was widely believed that ecologically important traits were too labile to be of much use in phylogenetic inference. The feeling was that such characters were so prone to homoplasy that they would be positively misleading about relationships; instead, one should concentrate on characters that lack obvious functional value [Mayr (1969) called this the ''Darwin principle'']. The rapid rise of the use of molecular data was partly a function of the belief that molecular characters were less subject to selection and would therefore better reflect evolutionary history. Arguments were made against this view on the grounds that it was hard to judge the phy-logenetic value of characters at the outset of an analysis [e.g., see Hennig (1966)]. However, in general, such arguments had rather little impact on the overall mindset; homoplasy was viewed as bad for phylogenetics and ''ecological traits'' were viewed as especially prone to homoplasy.

Where did this view come from? Within systematic biology one line of reasoning was that groups that were placed at higher taxonomic ranks (e.g., families, orders) showed little uniformity with respect to the environments that they occupied. This was said to be especially true in plants. For example, Arthur Cronquist, the prime architect of angiosperm classification in that era (from the 1960s through the 1980s), pointed out repeatedly that higher taxa were not readily characterized by particular ecological roles: ''Each of the obvious ecological niches for land plants is occupied by species representing diverse families and orders. . . . Conversely, a single family may fill widely varying ecological niches'' (Cronquist, 1968). Instead, higher taxa tended to be more uniform in minute details of their flowers and fruits, which remained constant through transitions into disparate environments. Cronquist referred especially to the Asteraceae (sunflower family) for support, noting that its members are marked by totally obvious reproductive characters, but vary from being trees, to shrubs, vines, succulents, and perennial and annual herbs, which grow from tidal to alpine zones, from the equator nearly to the poles. He concluded from such cases that ''the obvious adaptive changes that can take place mostly occur so easily and frequently that they tend to mark species and genera rather than larger groups'' (Cronquist, 1968).

Ledyard Stebbins, whose 1974 book on the macroevolution of flowering plants dominated discussions for decades, held much the same view. That is, he argued that owing ultimately to limited functional and developmental integration in plants, vegetative traits related to climate tolerances were highly labile and only rarely marked higher taxa. In fact, his main thesis depended directly on the rapidity with which transitions between major climate zones could occur. He argued that major evolutionary changes occurred in ecotones or climatically marginal zones, and that tropical rain forests were therefore ''museums,'' not ''cradles.'' As he appreciated, this required ''extreme ecological plasticity'' and genetic adaptation to moister or drier climates with ''relative ease'' (Stebbins, 1974).

Growing up with these views, and having passively accepted them, I remember being surprised by several later findings. Whereas I fully expected reproductive traits to show less homoplasy than vegetative traits that seemed to be linked more directly to climate variables (e.g., leaf margins, pubescence), a meta-analysis of homoplasy in published plant phylogenies failed to demonstrate such a difference (Donoghue and Sanderson, 1994). In fact, levels of homoplasy in phylogenetic studies rarely seem to correspond to standard intuitions about lability or selective value. Instead, homoplasy seems to be positively correlated primarily with the number of terminal taxa included in analyses [e.g., Sanderson and Donoghue (1989)] and limitations on the number of character states (Donoghue and Ree, 2000).

Even more surprising was the finding by Campbell Webb (2000) that the trees occupying 0.16-hectare plots in a rainforest in Borneo seemed to be more closely related to one another than expected by chance assembly from the regional species pool of 324 tree species. Given that these plots differed with respect to key environmental variables (some were located in swampy areas, some on ridge tops, etc.), one interpretation is that there are subtle, previously underappreciated, ecological similarities among related plants, both above and below the traditional rank of family. In retrospect, this can be reconciled with Cronquist's observations simply by allowing that shared ecological niche characteristics exist, but that the phylogenetic distribution of these does not correspond well with particular named clades or taxa assigned to a given taxonomic rank.

In general, comparisons centered on taxonomic ranks have hidden the connections between phylogeny and ecology. In fact, some tradi-

250 / Michael J. Donoghue tional taxonomic families are generally associated with particular environments; for example, Poaceae (the grasses) in grasslands, Ericaceae (the heaths) in heathlands, and Zosteraceae (the sea grasses) in the sea. The plant clade I know the best, the Dipsacales, ancestrally occupied northern temperate forests, but Dipsacaceae have specialized in drier habitats, especially around the Mediterranean basin, and Valerianaceae have adapted to alpine habitats (Donoghue et al., 2003). But there are also ecologically distinctive clades within traditional families: multiple mangrove lineages, dry-adapted Euphorbiaceae, and bamboos and multiple C4 lineages within grasses, to name just a few examples. Likewise, there are ecologically distinguishable clades comprised of a number of related families. Core Caryophyllales provide an example, mostly being adapted to arid or high-salinity habitats (e.g., the ''portulacaceous alliance'' of families, which includes the Cactaceae). The several insectivorous families within Carophyllales sensu lato present another clear case, as do those of the ''aquatic clade'' within Alismatales, and the parasitic plants of Santalales.

Moreover, it is important to appreciate that the findings of Webb (2000) and others (see below) do not depend on all members of a clade occupying the same habitat, but rather on a tendency for members of a clade to be more similar with respect to the environments that they occupy. From this perspective the link between phylogeny and ecology becomes even clearer. After all, major clades within angiosperms, despite significant ecological diversity, hardly occupy all possible environments, but instead are restricted to one or a few major biomes, such as tropical rainforests, temperate forests, grassland, or deserts. Despite the great variety of environments occupied by the Asteraceae, for example, they are far more common in arid environments than they are in tropical forests. Such tendencies are well known to field botanists, but have only recently been subjected to analysis. In the most comprehensive study to date, Prinzing et al. (2001) demonstrated far higher than expected levels of niche conservatism in the plants of Central Europe.

Such ecological correlations (especially those at the level of major clades) imply that evolutionary shifts from one ecological setting into another, where these require substantial physiological adjustments, are not so readily accomplished as one might have imagined, homoplasy in ecological traits notwithstanding. Consider one example: the evolution of cold tolerance. Many plant lineages have managed to adapt to cold, highly seasonal climates, but it is also true that only a subset of ancestrally tropical plant lineages have succeeded in making this transition (Judd et al., 1994). That is, many tropical plant groups are strictly tropical [e.g., half of the families of flowering plants have no temperate representatives; Ricklefs and Renner (1994)] and have not spread out of the tropics despite presumably having had ample opportunity to do so with the expansion of temperate climates (or the contraction of the tropics) during the Tertiary (Fine and Ree, 2006). The implication is that it is not so easy to evolve tolerance to freezing temperatures and highly seasonal environments. In fact, such adaptations do appear to require a coordinated set of physiological adjustments, including (in most cases) biochemical changes to maintain a fluid lipid layer for the rapid transfer of water out of cells to avoid ice crystals forming in the cytoplasm, and the deployment of special proteins and sugars to stabilize membranes when cells become desiccated and condensed (Sakai and Larcher, 1987; Korner, 2003).

Overall, my impression of ecological traits is that they show the same wide range in evolutionary lability as do morphological traits. On one end of the spectrum there are extremely labile traits of the sort that ecologists and population geneticists have tended to concentrate on. On the other end there are ecological traits of the sort I have highlighted above, which are evolutionarily much more conserved, perhaps because their evolution entails the modification of complex, highly integrated physiological systems. Recent phylogenetic studies have simply focused new light on the existence and the global importance of key ecological traits at the more conservative end of this distribution. My concentration here on the conserved end of the distribution is in no way meant to question the reality or significance of highly labile ecological traits, the evolution of which surely underlie many ecological adjustments.

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