The causes of evolvability and their evolution

Abstract

Evolvability is the ability of a biological system to produce phenotypic variation that is both heritable and adaptive. It has long been the subject of anecdotal observations and theoretical work. In recent years, however, the molecular causes of evolvability have been an increasing focus of experimental work. Here, we review recent experimental progress in areas as different as the evolution of drug resistance in cancer cells and the rewiring of transcriptional regulation circuits in vertebrates. This research reveals the importance of three major themes: multiple genetic and non-genetic mechanisms to generate phenotypic diversity, robustness in genetic systems, and adaptive landscape topography. We also discuss the mounting evidence that evolvability can evolve and the question of whether it evolves adaptively.

What drives phenotypic divergence among coral clonemates of Acropora palmata?

“…Interestingly, the abundance of two species of prokaryotes, Tepidiphilus and Endozoicomonas , differed among microbiome samples depending on their bleaching response and this supports findings that Endozoicomonas plays an important role in the functioning of the coral holobiont (Pollock et al, ). Ultradeep sequencing of host and symbionts may reveal the occurrence of somatic mutations in hosts (and/or symbionts) correlated with the bleaching phenotype (Van Oppen, Souter, Howells, Heyward, & Berkelmans, ) but nonmutation‐based mechanisms may also play a role (Goldsmith & Tawfik, ; Payne & Wagner, ), including detection‐based epigenetic modifications (sensu Shea, Pen, & Uller, ).…”

“…Plant researchers have made use of mutation accumulation lines grown under controlled conditions to make the distinction (e.g., Becker et al, ). Further, ultradeep sequencing of host and symbionts may reveal somatic mutations correlated with the bleaching phenotype (Van Oppen et al, ), although mechanisms other than detection‐based DNA methylation changes may also play a role (Goldsmith & Tawfik, ; Payne & Wagner, ), including selection‐based changes in epigenetic marks (Shea et al, ). Future work on this and other marine foundation species may significantly advance our understanding of these mechanisms in determining the evolvability of threatened species.…”

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

“…Indeed, by combining Wolpert's positional information with further patterning systems, either temporally or spatially, the overall robustness of the system might increase, and could thus be buffered against slight developmental deviations that eventually might transition into evolutionary novel patterns. 96,140 While variations in segment numbers are easily explained by alterations in the size or the temporal persistence of the progenitor pool, results from morphological extremes, like vertebral count in snakes or cetacean phalanges, suggest that different sub-modules of the system-for example the speed of an oscillator or proliferation-dependent feedback into the segmentation module-can be affected as well. 114,130 Moreover, size control between individual elements might be internally constrained by the molecular and/or cellular architecture of the ancestral segmentation process, thus restricting the exploration of the entire theoretically available morphospace.…”

Plasticity‐led evolution: A survey of developmental mechanisms and empirical tests

“…As an example of flexible regulation, consider that many signaling molecules and signal transducers can modify, inhibit, or promote (i.e., regulate) activities performed by other molecules, and that these regulatory molecules typically have numerous targets (Aharoni et al, 2005;Gordon & Nusse, 2006;Payne & Wagner, 2019;Payne, Moore, & Wagner, 2014). As an example of flexible regulation, consider that many signaling molecules and signal transducers can modify, inhibit, or promote (i.e., regulate) activities performed by other molecules, and that these regulatory molecules typically have numerous targets (Aharoni et al, 2005;Gordon & Nusse, 2006;Payne & Wagner, 2019;Payne, Moore, & Wagner, 2014).…”

“…For example, the diversity and abundance of trans regulatory variants (e.g., transcription factors, environmental sensors, noncoding RNAs, co-activating proteins, etc.) However, such flexible regulation can bias developmental and phenotypic possibilities insofar as any new developmental variants that arise are critically dependent on, and must be integrated with, existing variation, pathways, and networks (Payne & Wagner, 2019;Payne et al, 2014;Uller et al, 2018). This large mutational target space may increase the likelihood of a trait becoming decoupled from its environmental cue and/or experiencing various other modifications to its expression (Ehrenreich & Pfennig, 2016).…”