Natural Selection and Developmental Constraints in the Evolution of Allometries

Abstract

In animals, scaling relationships between appendages and body size exhibit high interspecific variation but low intraspecific variation. This pattern could result from natural selection for specific allometries or from developmental constraints on patterns of differential growth. We performed artificial selection on the allometry between forewing area and body size in a butterfly to test for developmental constraints, and then used the resultant increased range of phenotypic variation to quantify natural selection on the scaling relationship. Our results show that the shortterm evolution of allometries is not limited by developmental constraints. Instead, scaling relationships are shaped by strong natural selection.

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

“…At the whole‐eye level, changes in static allometric scaling relationships are restricted to grade shifts, with slope shifts entirely absent. This supports previous claims based on comparisons among closely related species or artificial selection experiments that allometric scaling relationships can evolve but that grade shifts are easier to achieve than slope shifts (Bolstad et al., 2015; Emlen & Nijhout, 2000; Frankino et al., 2005, 2007; Pélabon et al., 2014; Tobler & Nijhout, 2010; Toju & Sota, 2006; Voje et al., 2014). …”

“…Under artificial selection, Frankino et al. (2005, 2007) demonstrated that a genetically and functionally linked trait (hind‐wing size of a butterfly) can be forced into alternative scaling regimes, indicating that the restrictions on functionally linked morphological traits are not necessarily developmental/genetic (Mirth et al., 2016). Pélabon et al.…”

“…Grade shifts have been induced by artificial selection demonstrating that some aspects of allometric scaling can evolve rapidly (Bolstad et al., 2015; Frankino, Zwaan, Stern, & Brakefield, 2005, 2007). 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).…”

Realized correlated responses to artificial selection on pre-adult life-history traits in a butterfly

“…The measurement of constraints, however, has attracted substantial criticism and controversy (Gould and Lewinton, 1979;Pease and Bull, 1988;Houle, 1991;Stearns, 1992;Pigliucci and Kaplan, 2000;Sgrò and Hoffmann, 2004;Frankino et al, 2005). This is partly because there are many reasons for why an expected trade-off or constraint might not be found in practice, including variation in acquisition and allocation processes or variation in third traits in sufficiently complex multivariate systems (e.g.…”

How much do genetic covariances alter the rate of adaptation?

“…r 12 ZK0.5) will still allow for some adaptation-a fact noted by several investigators who have applied artificial selection to genetically correlated traits and still obtained a response to selection. These results come from agricultural systems (poultry : Nordskog 1977), model systems (mice : Cockrem 1959;Rutledge et al 1973) and evolutionary and ecological systems (flour and dung beetles, butterflies, and short-lived plants: Bell & Burris 1973;Stanton & Young 1994;Emlen 1996;Beldade et al 2002;Conner 2003;Frankino et al 2005). As such, the relevant comparison is not whether any adaptation can occur, but how much occurs relative to a scenario with a different covariance structure.…”