Abstract Animals use a diverse array of motion to feed, escape predators, and reproduce. Linking morphology, performance, and fitness is a foundational paradigm in organismal biology and evolution. Yet, the influence of mechanical relationships on evolutionary diversity remains unresolved. Here, I focus on the many-to-one mapping of form to function, a widespread, emergent property of many mechanical systems in nature, and discuss how mechanical redundancy influences the tempo and mode of phenotypic evolution. By supplying many possible morphological pathways for functional adaptation, many-to-one mapping can release morphology from selection on performance. Consequently, many-to-one mapping decouples morphological and functional diversification. In fish, for example, parallel morphological evolution is weaker for traits that contribute to mechanically redundant motions, like suction feeding performance, than for systems with one-to-one form–function relationships, like lower jaw lever ratios. As mechanical complexity increases, historical factors play a stronger role in shaping evolutionary trajectories. Many-to-one mapping, however, does not always result in equal freedom of morphological evolution. The kinematics of complex systems can often be reduced to variation in a few traits of high mechanical effect. In various different four-bar linkage systems, for example, mechanical output (kinematic transmission) is highly sensitive to size variation in one or two links, and insensitive to variation in the others. In four-bar linkage systems, faster rates of evolution are biased to traits of high mechanical effect. Mechanical sensitivity also results in stronger parallel evolution—evolutionary transitions in mechanical output are coupled with transition in linkages of high mechanical effect. In other words, the evolutionary dynamics of complex systems can actually approximate that of simpler, one-to-one systems when mechanical sensitivity is strong. When examined in a macroevolutionary framework, the same mechanical system may experience distinct selective pressures in different groups of organisms. For example, performance tradeoffs are stronger for organisms that use the same mechanical structure for more functions. In general, stronger performance tradeoffs result in less phenotypic diversity in the system and, sometimes, a slower rate of evolution. These macroevolutionary trends can contribute to unevenness in functional and lineage diversity across the tree of life. Finally, I discuss how the evolution of mechanical systems informs our understanding of the relative roles of determinism and contingency in evolution.
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When the end modifies its means: the origins of novelty and the evolution of innovation
The origin of novel complex traits constitutes a central yet largely unresolved challenge in evolutionary biology. Intriguingly, many of the most promising breakthroughs in understanding the genesis of evolutionary novelty in recent years have occurred not in evolutionary biology itself, but through the comparative study of development and, more recently, the interface of developmental biology and ecology. Here, I discuss how these insights are changing our understanding of what matters in the origin of novel, complex traits in ontogeny and evolution. Specifically, my essay has two major objectives. First, I discuss how the nature of developmental systems biases the production of phenotypic variation in the face of novel or stressful environments toward functional, integrated and, possibly, adaptive variants. This, in turn, allows the production of novel phenotypes to precede (rather than follow) changes in genotype and allows developmental processes that are the product of past evolution to shape evolutionary change that has yet to occur. Second, I explore how this nature of developmental systems has itself evolved over time, increasing the repertoire of ontogenies to pursue a wider range of objectives across an expanding range of conditions, thereby creating an increasingly extensive affordance landscape in development and developmental evolution. Developmental systems and their evolution can thus be viewed as dynamic processes that modify their own means across ontogeny and phylogeny. The study of these dynamics necessitates more than the strict reductionist approach that currently dominates the fields of developmental and evolutionary developmental biology.
more » « less- NSF-PAR ID:
- 10368722
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Biological Journal of the Linnean Society
- Volume:
- 139
- Issue:
- 4
- ISSN:
- 0024-4066
- Page Range / eLocation ID:
- p. 433-440
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Background A current argument in the CAM biology literature has focused on the nature of the CAM evolutionary trajectory: whether there is a smooth continuum of phenotypes between plants with C3 and CAM photosynthesis or whether there are discrete steps of phenotypic evolutionary change such as has been modelled for the evolution of C4 photosynthesis. A further implication is that a smooth continuum would increase the evolvability of CAM, whereas discrete changes would make the evolutionary transition from C3 to CAM more difficult.
Scope In this essay, I attempt to reconcile these two viewpoints, because I think in many ways this is a false dichotomy that is constraining progress in understanding how both CAM and C4 evolved. In reality, the phenotypic space connecting C3 species and strong CAM/C4 species is both a continuum of variably expressed quantitative traits and yet also contains certain combinations of traits that we are able to identify as discrete, recognizable phenotypes. In this sense, the evolutionary mechanics of CAM origination are no different from those of C4 photosynthesis, nor from the evolution of any other complex trait assemblage.
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