Many-to-One Mapping of Form to Function: A General Principle in Organismal Design?
2005/04/01 by P. C. Wainwright, Peter C. Wainwright · 59 citations
Earth and Planetary Sciences · Environmental Science · #Evolution and Paleontology Studies #Paleontology and Evolutionary Biology #Ichthyology and Marine Biology
paper · pdf · doi:10.1093/icb/45.2.256
Abstract
We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R(2) = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.
Cited by
- Divergence time shapes gene reuse during repeated adaptation
- Trait Multi-Functionality in Plant Stress Response
- Salamander ecomorphology reveals a unique suite of climbing adaptations
- Bone structure and the evolution of different pathways to gigantism in dinosaurs and megamammals
- BIOTIC INTERACTIONS AND MACROEVOLUTION: EXTENSIONS AND MISMATCHES ACROSS SCALES AND LEVELS
- The ecology of a continental evolutionary radiation: Is the radiation of sigmodontine rodents adaptive?
- Rare ecomorphological convergence on a complex adaptive landscape: Body size and diet mediate evolution of jaw shape in squirrels (Sciuridae)
- Functional performance of turtle humerus shape across an ecological adaptive landscape
- Locomotor performance constrained by morphology and habitat in a diverse clade of African frogs (Anura: Pyxicephalidae)
- Replicated Functional Evolution in Cichlid Adaptive Radiations
- Evolution of ecospace occupancy by Mesozoic marine tetrapods
- Quantitative discrimination of flightlessness in fossil Anatidae from skeletal proportions
- The Carnivoran Adaptive Landscape Reveals Trade-offs among Functional Traits in the Skull, Appendicular, and Axial Skeleton
- The Life History of Whole-Organism Performance
- Comparative muscle anatomy of the anuran pelvis and hindlimb in relation to locomotor mode
- Many ways to build an angler: diversity of feeding morphologies in a deep-sea evolutionary radiation
- Frog Fibres: What Muscle Architecture Can Tell Us About Anuran Locomotor Function
- Macroevolutionary changes in gene expression response to an immune stimulus across the diversity of fishes
- The carnivoran adaptive landscape reveals functional trade-offs among the skull, appendicular, and axial skeleton
- Brawn before bite in endemic Asian eutherian mammals after the end-Cretaceous extinction
- Convergent Evolution of Claw Shape in a Transcontinental Lizard Radiation
- Champsosaurs, gharials, and the functional ecomorphology of resource partitioning
- Phylogenetic community structure in Minnesota oak savanna is influenced by spatial extent and environmental variation
- Clinging strength, but not sprint speed, underlies morphological divergence between ecologically distinct <i>Liolaemus</i> species
- Drivers and mechanisms of convergent forelimb reduction in non-avian theropod dinosaurs
- Biomechanical Specialization Acts as an Asymmetrical Constraint on the Phenotype
- Genes, Morphology, Performance, and Fitness: Quantifying Organismal Performance to Understand Adaptive Evolution
- Evolution of the Gekkotan Adhesive System: Does Digit Anatomy Point to One or More Origins?
- Contingency and determinism in evolution: Replaying life’s tape
- Four-bar Geometry is Shared among Ecologically DivergentFish Species
- Optimal Gearing of Musculoskeletal Systems
- Wing Musculature Reconstruction in Extinct Flightless Auks ( <i>Pinguinus</i> and <i>Mancalla</i> ) Reveals Incomplete Convergence with Penguins (Spheniscidae) Due to Differing Ancestral States
- Comparative morpho‐functional analysis of the humerus and ulna in three Western European moles species of the genus <i>Talpa</i>, including the newly described <i>T. aquitania</i>
- What Can Computational Modeling Tell Us about the Diversity of Odor-Capture Structures in the Pancrustacea?
- Hybridization produces novelty when the mapping of form to function is many to one. [europepmc]
- Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. [europepmc]
- Heads or tails: staged diversification in vertebrate evolutionary radiations. [europepmc]
- Adaptive evolution of facial colour patterns in Neotropical primates. [europepmc]
- Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. [europepmc]
- Does morphological convergence imply functional similarity? A test using the evolution of quadrupedalism in ornithischian dinosaurs. [europepmc]
- Morphological and biomechanical disparity of crocodile-line archosaurs following the end-Triassic extinction. [europepmc]
- Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. [europepmc]
- Functional basis of ecological divergence in sympatric stickleback. [europepmc]
- Mechanical analysis of avian feet: multiarticular muscles in grasping and perching. [europepmc]
- Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use. [europepmc]
- Mechanical sensitivity and the dynamics of evolutionary rate shifts in biomechanical systems. [europepmc]
- Dynamic Musculoskeletal Functional Morphology: Integrating diceCT and XROMM. [europepmc]
- Specialized specialists and the narrow niche fallacy: a tale of scale-feeding fishes. [europepmc]
- Pterosaur dietary hypotheses: a review of ideas and approaches. [europepmc]
- Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities. [europepmc]
- Strong biomechanical relationships bias the tempo and mode of morphological evolution. [europepmc]
- Raptor talon shape and biomechanical performance are controlled by relative prey size but not by allometry. [europepmc]
- The Evolutionary Dynamics of Mechanically Complex Systems. [europepmc]
- Interspecific hybridization can generate functional novelty in cichlid fish. [europepmc]
- Evolution of a multifunctional trait: shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution. [europepmc]
- Disparities in the analysis of morphological disparity. [europepmc]
- Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants. [europepmc]
- The Effect of Locomotion Mode on Body Shape Evolution in Teleost Fishes. [europepmc]
- A switch in jaw form-function coupling during the evolution of mammals. [europepmc]
Related