Evolvability: progress and key questions

Abstract

Since the 1990s, evolutionary biologists have recognized the importance of explaining the ability of biological systems to evolve and how this ability itself evolves. This recognition of the need to explain evolvability emerged from an awareness that the kind and the amount of heritable variation available for natural selection require explanation. The concept of evolvability is now the focus of many research programs in diverse subdisciplines within evolutionary biology. In the present article, we first review and synthesise progress made in evolvability research. We then present key questions to set an agenda for future research on evolvability, identify challenges to answer these questions, and discuss opportunities to apply results from the evolvability research to conservation biology.

Keywords: evo-devo; evolutionary quantitative genetics; evolutionary systems biology; evolvability; paleobiology.

Figure 1.

Example of evolutionary questions involving evolvability. (a) Species of cichlids in lake Tanganyika differ extensively in their craniofacial morphology and in their feeding regimes. Galis and Drucker (1996) suggested that the evolution of such diversity was made possible by developmental changes that allowed independent movements of the upper and lower pharyngeal jaws, thereby increasing the evolvability of the feeding apparatus. (b) Although almost all mammalian species have only seven cervical vertebrae whatever the length of their neck, bird species differ extensively in the number of cervical vertebrae; this allows the evolution of long and flexible neck, as in flamingoes. Why is the number of cervical vertebrae not evolvable in mammals? Galis (2023) suggested that the constraint in mammals results from the deleterious pleiotropic effects associated with changes in the induction of cervical vertebrae. (c) O'Meara and colleagues (2016) showed that clades with bilateral flowers (e.g., Orchis purpurea, Orchidaceae, left) contain many more species than clades with radial flowers (e.g., Sempervivum montanum, Crassulaceae, right). Whether this results from differences in the selection pressures generated by specialist or from generalist pollinators or from differences in evolvability remains unresolved (Woźniak and Sicard 2018). (d) The morphology of the horseshoe crabs (Xiphosurida) has changed little since the Jurassic. Whether this lack of evolution can be explained by natural selection or by low evolvability is unresolved (Bicknell et al. 2022). (e) The allometric relationship between antler size and body size in cervids, with the iconic Megaloceros, is a key example of evolutionary constraints where body size and antler size are supposedly forced to evolve along a trajectory imposed by the development (Gould , Tsuboi et al. 2024). However, the low evolvability in static allometric slopes but the high evolvability in static allometric intercepts (Bolstad et al. 2015) suggest that allometric constraints alone cannot fully explain the origin of evolutionary allometry observed in deer antlers and in many other systems. Sources: (a) from Albertson and Kocher ; (b) from Galis (http://creativecommons.org/licenses/by/4.0), left reproduced from Owen (1866), and right reproduced from Evans. Photographs: (c) Christophe Pélabon, (d) Didier Descouens, (e) Tsuboi et al. (http://creativecommons.org/licenses/by/4.0)

Figure 2.

Evolvability at different biological and temporal scales. Top row: levels at which variation in evolvability can be studied. Second row: mechanisms affecting evolvability. Third row: evolvability measures or proxies for it at different organismal levels and timescales (V_A, additive genetic variance; I_A, mean-scaled evolvability; V_M, mutational variance). Fourth row: evolutionary events expected to be affected by evolvability, and therefore how variation in evolvability is expressed (µ, population mean). Last row: typical bearers of evolvability.

Figure 3.

Linear and nonlinear genotype–phenotype maps (GP map), directional epistasis and evolvability. (a) A linear GP map where the black line represents the function that is mapping genetic variation, represented by bell curves on the x-axis, onto heritable phenotypic variation represented by bell curves on the y-axis. In this GP map, a genetic change in the DNA sequence that increases (the red arrows toward right) or decreases (the blue arrows toward left) the trait has always the same effect on the phenotype whatever the direction of the change and the genetic background in which it occurs (different genotypes on the x-axis correspond to different genetic background). With a such GP map, evolvability, which depends on heritable variation, remains constant when the trait evolves. (b) A nonlinear GP map where the phenotypic effect of a given genetic change depends on the direction of the change and the genetic background in which it occurs. For example, in the right half of the curve, the effect of a genetic change that increases the trait value diminishes when the trait increases (the red arrows on the y-axis decrease when the trait mean is moving toward its maximum value represented by the dashed line). This implies that genetic changes that increase the trait will decrease the effect of other genetic changes that also increase the trait, a mechanism referred to as negative directional epistasis. With directional epistasis, evolvability changes with the trait mean. (c) A possible example of negative directional epistasis in the artificial selection on maximum heat tolerance (CT_max) in zebrafish. The red lines and symbols (above the dash line) represent the response of the lines selected for an increase in CT_max, and the blue lines and symbols (below the dash line) represent the response of the lines to decrease CT_max (as compared with the control lines). The highly asymmetrical response to selection is possibly generated by biochemical limits at high temperature (Morgan et al. 2020). (d) Possible effect of environmental variation, represented by acclimation, on evolvability in the presence of negative directional epistasis. With acclimation, CT_max generally increases but shows less phenotypic and genetic variation. Source: Panels (c) and (d) were drawn from Morgan and colleagues (2020).