Allometric Constraints and the Evolution of Allometry

Abstract

Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within-species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million-year, cross-species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait-size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow-sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable. K E Y W O R D S :Adaptation, evolutionary constraint, microevolution, macroevolution, ontogenetic allometry, static allometry.

Conservative whole‐organ scaling contrasts with highly labile suborgan scaling differences among compound eyes of closely related Formica ants

“…Changes can occur in both intercept, referred to as grade shifts, and/or power, referred to as slope shifts. Scaling relationships can be classified in one of three principle ways (Cock, 1966; Gould, 1966): (1) ontogenetic allometry, which characterizes how an organ changes size as an organism develops (McLellan et al., 2002); (2) static allometry, which compares organ scaling among conspecifics at a given stage of development (typically adulthood; McCullough, Ledger, O'Brien, & Emlen, 2015); and (3) phylogenetic or evolutionary allometry, which compares the scaling of homologous/analogous structures between related species at a given taxonomic level (Voje, Hansen, Egset, Bolstad, & Pélabon, 2014). …”

“…Despite these proposed limitations, however, there is substantial evidence showing that allometric scaling relationships can evolve (Emlen & Nijhout, 2000; Voje et al., 2014). This is supported by comparisons of static allometries that show they can differ within populations (Perl & Niven, 2016a), and among populations and species (Emlen & Nijhout, 2000; McGuigan, Nishimura, Currey, Hurwit, & Cresko, 2010; Simmons & Tomkins, 1996; Toju & Sota, 2006; Weber, 1990).…”

“…In contrast to the wealth of evidence demonstrating that intercepts can evolve, allometric slopes appear more constrained in their evolution, many organs showing remarkably little variation in scaling exponents between species separated by millions of years (Voje et al., 2014). Those experiments that have attempted to artificially select for slope shifts (Bolstad et al., 2015; Egset et al., 2012; Frankino et al., 2007; Stillwell, Shingleton, Dworkin, & Frankino, 2016; Tobler & Nijhout, 2010) have been criticized because of the methodology they employ (Mirth et al., 2016; Stillwell et al., 2016).…”

Why the short face? Developmental disintegration of the neurocranium drives convergent evolution in neotropical electric fishes

“…Heterocephaly describes a particular pattern of inversely correlated shape changes associated with neurocranial size involving a relative contraction (negative allometry) of the braincase and relative elongation (positive allometry) of the face or snout regions of the skull. By this definition, heterocephaly can refer to neurocranial allometries during growth of a single individual, among individuals of different sizes within a population, among adults of different populations within a species, or among adults between different species, that is, ontogenetic, static, or evolutionary allometries (Voje & Hansen, 2013; Voje et al., 2014). Heterocephalic patterns of variation and diversity have been reported in several other taxa (Tables S4 and S5).…”

“…Specimens were also selected to represent as large a range of body sizes as possible from among available materials. This approach does however confound static and ontogenetic allometry as it captures all shape variation associated with size and not just the shape variation associated with growth (Pélabon et al., 2014; Voje & Hansen, 2013; Voje, Hansen, Egset, Bolstad, & Pelabon, 2014). For most species, these specimens range in size from posthatching juveniles just at the onset of bone mineralization, to morphologically mature adults >90% maximum known total length.…”