Evolvability and nonevolvability of allometric slopes

The science of morphological allometry centers around relationships between the size of organismal structures and overall body size. Morphological allometry usually is concerned with two parameters, the slope of log–log plots of trait parameters on body mass or size (reflecting how trait size varies with body size), and the intercept of such plots (providing measures of body-size–independent trait parameters). Morphological allometry is a central area of study for organismal and evolutionary biologists, because body size explains a large proportion of the variance in size of most body structures, and because we still lack a broad mechanistic understanding of the processes that produce allometric slopes. One of the debated themes of allometric research has been whether allometric slopes are determined by natural selection or represent constraints on biological variation. In PNAS, Bolstad et al. (1) address this question directly by testing whether the allometric slope of wing vein length on wing area of Drosophila melanogaster could be changed by artificial selection (yes, it was changed), and also show that after selection on allometric slopes, but not their intercepts, populations returned rapidly to control values when artificial selection ceased (Fig. 1). Bolstad et al. conclude that the rapid return of allometric slope to control values provides evidence for a pleiotropic constraint on the slope; that is, the genetic, developmental, and functional bases for different traits are not independent, so that selection on one allometric relationship affects others and overall fitness. They state “… this hypothesis could provide a general explanation for the striking evolutionary conservatism of allometric power laws, while still leaving open the possibility for allometries to be optimized by natural selection over long time scales through compensatory mutations” (1).

Fig. 1.

Bolstad et al. (1) used a saddle-function as a selection index and disassortative mating between large and small flies to increase the allometric slope while minimizing linkage disequilibrium. Conversely, matings between short-winged large flies and relatively long-winged small flies depressed the allometric slope.

Allometry can be studied during ontogeny, within populations for individuals at a specific developmental stage (static allometry) and across populations or species (evolutionary allometry). Understanding the relationships across these different scales is critical for development of unifying theories that integrate between proximate mechanisms and our understanding of evolutionary allometries because, to some extent, allometries at higher levels of organization depend on allometries at the lower level (2, 3). Bolstad et al. (1) first compared the interspecific and within-species allometric relationships for 111 Drosophilid species. Across and within species, as wings become larger, the L2 wing vein intersects the leading edge of the wing more distally; that is, log–log plots of the L2 vein length on the square root of wing area have slopes >1. For reasons that are unclear, this trend (and the slope of the log–log plot) is greater for interspecific comparisons than within populations. Evolutionary changes in the allometric slope were less than 2.8% per million y, showing that although the slope can evolve, there is strong conservation of these relationships.

Artificial selection for relatively long or short wing veins at a given body size was able to change the intercept of the static allometric lines by 6–9% in only seven generations. Importantly, these changes were relatively stable after selection stopped, with only a 15% reversion toward control values over 16 generations, suggesting that wing shape was not under strong selection in these cultures. Artificial selection on the allometric slope was also successful, with “up-selection” increasing the slope to a value nearly 30% above control values, and “down-selection” decreasing the slope to a value about 75% of the control slope. These selected populations had allometric slopes similar to the most extreme Drosophilid species. However, unlike for the populations that had been selected for long or short veins at a given wing size, these slopes reverted quickly to control values within 14 generations. Bolstad et al. (1) suggest that the rapid reversion of the allometric slope indicates that the allometric relationship between vein length and wing size is under strong selection. Allometric slopes have long been considered to impact function, and thus be subject to ecological selection (4). However, the fact that flies with high or low vein length:wing size could persist for many generations after selection suggests that all of these wing shapes function adequately, at least in the laboratory culture environment. Thus, Bolstad et al. (1) suggest that the selection that returned the allometric slope to control values was mediated by a pleotropic developmental constraint.

What do these results imply for broader questions in allometry? First, this is a unique experimental demonstration of the possibility for the allometric slope to evolve, supporting results of many comparative studies that document substantial variation in allometric slopes (4, 5). A major thrust of recent studies in morphological allometry has been development of an understanding of the mechanisms of individual plasticity of response to body size. These studies have focused on two common patterns: the tendency for large males of some species to have exaggerated sexually selected traits, such as giant horns of some beetles or large antlers of some cervids, and also the tendency for the genitalia of arthropods to be preserved in size across a wide range of body sizes (6). An emerging model is that tissues that are relatively enlarged in more massive animals have endocrine signaling systems (such as insulin signaling systems) that are more responsive to circulating growth-stimulating factors than other tissues (7). Although to date these pathways have only been demonstrated for plastic changes in slopes, it is certainly conceivable

One of the debated themes of allometric research has been whether allometric slopes are determined by natural selection or represent constraints on biological variation.

that organ-specific variation in responsiveness to growth-promoting neuroendocrine signals is heritable and could provide a mechanism allowing variation in allometric slopes across populations and species.

Bolstad et al. (1) emphasize the importance of the apparent constraints on such allometric slopes, pointing out correctly that most morphological traits exhibit tight allometric relationships with body size; this is strikingly true in the Drosophila wing despite the occurrence of additive genetic variance in 20 aspects of wing structure (8). Their finding calls for examination of the possible developmental mechanisms that might cause differential survival of individuals with extreme allometries. Conducting such quantitative genetic approaches with structures and processes that are likely less tightly linked is also merited. Wing veins are structural components of wing area, increasing the likelihood of finding constraints on relative proportions. The most interesting aspects of allometry that drive major changes in life histories are traits with less obvious morphological links with body size. Brain size and metabolic rate both scale hypometrically with body mass, with strong effects on a myriad of life history traits (9–11). Plausibly, models in which the allometric slopes of metabolic rates are determined by the scaling of surface areas or branching supply structures could be subject to such pleiotropic developmental constraints. Distinguishing such constraints from size-dependent selection remains a major goal of organismal and evolutionary biology.