An official website of the United States government
Since Darwin, biologists have sought to understand the evolution and origins of phenotypic adaptations. The skull is particularly diverse due to intense natural selection on feeding biomechanics. We investigated the genetic and molecular origins of trophic adaptation using Lake Malawi cichlids, which have undergone an exemplary evolutionary radiation. We analyzed morphological differences in the lateral and ventral head shape among an insectivore that eats by suction feeding, an obligate biting herbivore, and their F2 hybrids. We identified variation in a series of morphological traits—including mandible width, mandible length, and buccal length—that directly affect feeding kinematics and function. Using quantitative trait loci (QTL) mapping, we found that many genes of small effects influence these craniofacial adaptations. Intervals for some traits were enriched in genes related to potassium transport and sensory systems, the latter suggesting co-evolution of feeding structures and sensory adaptations for foraging. Despite these indications of co-evolution of structures, morphological traits did not show covariation. Furthermore, phenotypes largely mapped to distinct genetic intervals, suggesting that a common genetic basis does not generate coordinated changes in shape. Together, these suggest that craniofacial traits are mostly inherited as separate modules, which confers a high potential for the evolution of morphological diversity. Though these traits are not restricted by genetic pleiotropy, functional demands of feeding and sensory structures likely introduce constraints on variation. In all, we provide insights into the quantitative genetic basis of trophic adaptation, identify mechanisms that influence the direction of morphological evolution, and provide molecular inroads to craniofacial variation.
more »
« less
The Evolutionary Dynamics of Mechanically Complex Systems
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.
more »
« less
- Award ID(s):
- 1839250
- PAR ID:
- 10170997
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 3
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 705 to 715
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
A central challenge for biology is to reveal how different levels of biological variation interact and shape diversity. However, recent experimental studies have indicated that prevailing models of evolution cannot readily explain the link between micro- and macroevolution at deep timescales. Here, we suggest that this paradox could be the result of a common mechanism driving a correlated pattern of evolution. We examine the proportionality between genetic variance and patterns of trait evolution in a system whose developmental processes are well understood to gain insight into how such alignment between morphological divergence and genetic variation might be maintained over macroevolutionary time. Primate molars present a model system by which to link developmental processes to evolutionary dynamics because of the biased pattern of variation that results from the developmental architecture regulating their formation. We consider how this biased variation is expressed at the population level, and how it manifests through evolution across primates. There is a strong correspondence between the macroevolutionary rates of primate molar divergence and their genetic variation. This suggests a model of evolution in which selection is closely aligned with the direction of genetic variance, phenotypic variance, and the underlying developmental architecture of anatomical traits.more » « less
-
Abstract Approaches to macroevolution require integration of its two fundamental components, i.e. the origin and the sorting of variation, in a hierarchical framework. Macroevolution occurs in multiple currencies that are only loosely correlated, notably taxonomic diversity, morphological disparity, and functional variety. The origin of variation within this conceptual framework is increasingly understood in developmental terms, with the semi-hierarchical structure of gene regulatory networks (GRNs, used here in a broad sense incorporating not just the genetic circuitry per se but the factors controlling the timing and location of gene expression and repression), the non-linear relation between magnitude of genetic change and the phenotypic results, the evolutionary potential of co-opting existing GRNs, and developmental responsiveness to nongenetic signals (i.e. epigenetics and plasticity), all requiring modification of standard microevolutionary models, and rendering difficult any simple definition of evolutionary novelty. The developmental factors underlying macroevolution create anisotropic probabilities—i.e., an uneven density distribution—of evolutionary change around any given phenotypic starting point, and the potential for coordinated changes among traits that can accommodate change via epigenetic mechanisms. From this standpoint, “punctuated equilibrium” and “phyletic gradualism” simply represent two cells in a matrix of evolutionary models of phenotypic change, and the origin of trends and evolutionary novelty are not simply functions of ecological opportunity. Over long timescales, contingency becomes especiallyimportant, and can be viewed in terms of macroevolutionary lags (the temporal separation between the origin of a trait or clade and subsequent diversification); such lags can arise by several mechanisms: as geological or phylogenetic artifacts, or when diversifications require synergistic interactions among traits, or between traits and external events. The temporal and spatial patterns of the origins of evolutionary novelties are a challenge to macroevolutionary theory; individual events can be described retrospectively, but a general model relating development, genetics, and ecology is needed. An accompanying paper (Jablonski in Evol Biol 2017) reviews diversity dynamics and the sorting of variation, with some general conclusions.more » « less
-
Abstract Approaches to macroevolution require integration of its two fundamental components, within a hierarchical framework. Following a companion paper on the origin of variation, I here discuss sorting within an evolutionary hierarchy. Species sorting—sometimes termed species selection in the broad sense, meaning differential origination and extinction owing to intrinsic biological properties—can be split into strict-sense species selection, in which rate differentials are governed by emergent, species-level traits such as geographic range size, and effect macroevolution, in which rates are governed by organism-level traits such as body size; both processes can create hitchhiking effects, indirectly causing the proliferation or decline of other traits. Several methods can operationalize the concept of emergence, so that rigorous separation of these processes is increasingly feasible. A macroevolutionary tradeoff, underlain by the intrinsic traits that influence evolutionary dynamics, causes speciation and extinction rates to covary in many clades, resulting in evolutionary volatility of some clades and more subdued behavior of others; the few clades that break the tradeoff can achieve especially prolific diversification. In addition to intrinsic biological traits at multiple levels, extrinsic events can drive the waxing and waning of clades, and the interaction of traits and events are difficult but important to disentangle. Evolutionary trends can arise in many ways, and at any hierarchical level; descriptive models can be fitted to clade trajectories in phenotypic or functional spaces, but they may not be diagnostic regarding processes, and close attention must be paid to both leading and trailingedges of apparent trends. Biotic interactions can have negative or positive effects on taxonomic diversity within a clade, but cannot be readily extrapolated from the nature of such interactions at the organismic level. The relationships among macroevolutionary currencies through time (taxonomic richness, morphologic disparity, functional variety) are crucial for understanding the nature of evolutionary diversification. A novel approach to diversity-disparity analysis shows that taxonomic diversifications can lag behind, occur in concert with, or precede, increases in disparity. Some overarching issues relating to both the origin and sorting of clades and phenotypes include the macroevolutionary role of mass extinctions, the potential differences between plant and animal macroevolution, whether macroevolutionary processes have changed through geologic time, and the growing human impact on present-day macroevolution. Many challenges remain, but progress is being made on two of the key ones: (a) the integration of variation-generating mechanisms and the multilevel sorting processes that act on that variation, and (b) the integration of paleontological and neontological approaches to historical biology.more » « less
-
Synopsis The concept of modularity is fundamental to understanding the evolvability of morphological structures and is considered a central framework for the exploration of functionally and developmentally related subsets of anatomical traits. In this study, we explored evolutionary patterns of modularity and integration in the 4-bar linkage biomechanical system of the skull in the fish family Labridae (wrasses and parrotfishes). We measured evolutionary modularity and rates of shape diversification of the skull partitions of three biomechanical 4-bar linkage systems using 205 species of wrasses (family: Labridae) and a three-dimensional geometric morphometrics data set of 200 coordinates. We found support for a two-module hypothesis on the family level that identifies the bones associated with the three linkages as being a module independent from a module formed by the remainder of the skull (neurocranium, nasals, premaxilla, and pharyngeal jaws). We tested the patterns of skull modularity for four tribes in wrasses: hypsigenyines, julidines, cheilines, and scarines. The hypsigenyine and julidine groups showed the same two-module hypothesis for Labridae, whereas cheilines supported a four-module hypothesis with the three linkages as independent modules relative to the remainder of the skull. Scarines showed increased modularization of skull elements, where each bone is its own module. Diversification rates of modules show that linkage modules have evolved at a faster net rate of shape change than the remainder of the skull, with cheilines and scarines exhibiting the highest rate of evolutionary shape change. We developed a metric of linkage planarity and found the oral jaw linkage system to exhibit high planarity, while the rest position of the hyoid linkage system exhibited increased three dimensionality. This study shows a strong link between phenotypic evolution and biomechanical systems, with modularity influencing rates of shape change in the evolution of the wrasse skull.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz077
