Development shapes the evolutionary diversification of rodent stripe patterns

Significance

How and why did diverse animal color patterns evolve? Explanations for pattern diversification typically emphasize the ecological forces that select for color patterns (e.g., camouflage or sexual selection). However, pattern diversification may also critically depend on the developmental mechanisms that provide the substrate for pattern evolution. Here, drawing on empirical advances, we explore theoretically how development shapes rodent pattern diversification. We show that pattern diversification can indeed be partly explained by underlying developmental mechanisms. Specifically, development can both facilitate and constrain pattern evolution by enabling evolutionary changes in stripe number while limiting changes in stripe positioning. Thus, by integrating developmental data, models of pattern formation, and empirical data on pattern diversity, our work helps bridge the gap between pattern evolution and pattern development.

Abstract

Vertebrate groups have evolved strikingly diverse color patterns. However, it remains unknown to what extent the diversification of such patterns has been shaped by the proximate, developmental mechanisms that regulate their formation. While these developmental mechanisms have long been inaccessible empirically, here we take advantage of recent insights into rodent pattern formation to investigate the role of development in shaping pattern diversification across rodents. Based on a broad survey of museum specimens, we first establish that various rodents have independently evolved diverse patterns consisting of longitudinal stripes, varying across species in number, color, and relative positioning. We then interrogate this diversity using a simple model that incorporates recent molecular and developmental insights into stripe formation in African striped mice. Our results suggest that, on the one hand, development has facilitated pattern diversification: The diversity of patterns seen across species can be generated by a single developmental process, and small changes in this process suffice to recapitulate observed evolutionary changes in pattern organization. On the other hand, development has constrained diversification: Constraints on stripe positioning limit the scope of evolvable patterns, and although pattern organization appears at first glance phylogenetically unconstrained, development turns out to impose a cryptic constraint. Altogether, this work reveals that pattern diversification in rodents can in part be explained by the underlying development and illustrates how pattern formation models can be leveraged to interpret pattern evolution.