Many‐to‐one form‐to‐function mapping weakens parallel morphological evolution

Abstract

Evolutionary ecologists aim to explain and predict evolutionary change under different selective regimes. Theory suggests that such evolutionary prediction should be more difficult for biomechanical systems in which different trait combinations generate the same functional output: "many-to-one mapping." Many-to-one mapping of phenotype to function enables multiple morphological solutions to meet the same adaptive challenges. Therefore, many-to-one mapping should undermine parallel morphological evolution, and hence evolutionary predictability, even when selection pressures are shared among populations. Studying 16 replicate pairs of lake- and stream-adapted threespine stickleback (Gasterosteus aculeatus), we quantified three parts of the teleost feeding apparatus and used biomechanical models to calculate their expected functional outputs. The three feeding structures differed in their form-to-function relationship from one-to-one (lower jaw lever ratio) to increasingly many-to-one (buccal suction index, opercular 4-bar linkage). We tested for (1) weaker linear correlations between phenotype and calculated function, and (2) less parallel evolution across lake-stream pairs, in the many-to-one systems relative to the one-to-one system. We confirm both predictions, thus supporting the theoretical expectation that increasing many-to-one mapping undermines parallel evolution. Therefore, sole consideration of morphological variation within and among populations might not serve as a proxy for functional variation when multiple adaptive trait combinations exist.

Asymmetric Isolation and the Evolution of Behaviors Influencing Dispersal: Rheotaxis of Guppies above Waterfalls

“…Positive rheotaxis is therefore a "performance" metric that could be achieved through multiple different behavioral, physiological, or morphological solutions. Thus, the problem of evolving positive rheotaxis in above-waterfall populations is another example of many-to-one mapping [25]. In such cases, a key question becomes whether parallel evolution of performance (positive rheotaxis) is the result of non-parallel solutions.…”

A biomechanical analysis of prognathous and orthognathous insect head capsules: evidence for a many‐to‐one mapping of form to function

“…Also, the significance of morphological change could be overestimated if morphological evolution is functionally neutral. A widely studied example of MTOM is the four-bar linkage of the feeding apparatus of labrid fish, where the four bony elements have different lengths but map onto a similar mechanical performance space (Alfaro et al, 2004;Parnell et al, 2008;Cooper & Westneat, 2009;Martinez & Sparks, 2017;Thompson et al, 2017). However, there are many instances where feeding systems show more fundamental morphological differences despite similar food sources, and thus the ways of morphological optimization to similar performance spaces might be difficult to detect.…”

Exploring the functional meaning of head shape disparity in aquatic snakes

“…However, this relationship is not always straightforward as demonstrated by the phenomenon of many-to-one mapping of form to function, with different morphologies giving rise to similar levels of performance (Stayton, 2011; Wainwright, Alfaro, Bolnick, & Hulsey, 2005). Furthermore, many-to-one mapping appears to weaken the evidence for parallel evolution among species sharing similar ecological features (Stuart et al, 2017; Thompson et al, 2017), which adds complexity to form-function-ecology relationship. Thus, in order to understand the origin of shape disparity in organisms that demonstrate parallel evolution, we need to investigate the interplay between ecological and functional constraints.…”

“…The feeding apparatus of fully aquatic vertebrates, such as fish, either has morphologically or functionally converged (i.e. many-to-one-mapping) in response to the hydrodynamic constraints involved during prey capture (Collar & Wainwright, 2006; Cooper et al, 2010; Stuart et al, 2017; Thompson et al, 2017; Wainwright et al, 2005; Winemiller, Kelso-Winemiller, & Brenkert, 1995). In the present study, we propose to investigate the interplay between different selective pressures that may generate shape diversity (i.e.…”