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Abstract
Natural selection acts on phenotypes constructed over development, which raises the question of how development affects evolution. Classic evolutionary theory indicates that development affects evolution by modulating the genetic covariation upon which selection acts, thus affecting genetic constraints. However, whether genetic constraints are relative, thus diverting adaptation from the direction of steepest fitness ascent, or absolute, thus blocking adaptation in certain directions, remains uncertain. This limits understanding of longterm evolution of developmentally constructed phenotypes. Here we formulate a general, tractable mathematical framework that integrates age progression, explicit development (i.e., the construction of the phenotype across life subject to developmental constraints), and evolutionary dynamics, thus describing the evolutionary and developmental (evodevo) dynamics. The framework yields simple equations that can be arranged in a layered structure that we call the evodevo process, whereby five core elementary components generate all equations including those mechanistically describing genetic covariation and the evodevo dynamics. The framework recovers evolutionary dynamic equations in gradient form and describes the evolution of genetic covariation from the evolution of genotype, phenotype, environment, and mutational covariation. This shows that genotypic and phenotypic evolution must be followed simultaneously to yield a dynamically sufficient description of longterm phenotypic evolution in gradient form, such that evolution described as the climbing of a fitness landscape occurs in “genophenotype” space. Genetic constraints in genophenotype space are necessarily absolute because the phenotype is related to the genotype by development. Thus, the longterm evolutionary dynamics of developed phenotypes is strongly nonstandard: (1) evolutionary equilibria are either absent or infinite in number and depend on genetic covariation and hence on development; (2) developmental constraints determine the admissible evolutionary path and hence which evolutionary equilibria are admissible; and (3) evolutionary outcomes occur at admissible evolutionary equilibria, which do not generally occur at fitness landscape peaks in genophenotype space, but at peaks in the admissible evolutionary path where “total genotypic selection” vanishes if exogenous plastic response vanishes and mutational variation exists in all directions of genotype space. Hence, selection and development jointly define the evolutionary outcomes if absolute mutational constraints and exogenous plastic response are absent, rather than the outcomes being defined only by selection. Moreover, our framework provides formulas for the sensitivities of a recurrence and an alternative method to dynamic optimization (i.e., dynamic programming or optimal control) to identify evolutionary outcomes in models with developmentally dynamic traits. These results show that development has major evolutionary effects.
Original language  English 

Pages (fromto)  2450 
Number of pages  27 
Journal  Theoretical Population Biology 
Volume  155 
Early online date  13 Dec 2023 
DOIs  
Publication status  Published  Feb 2024 
Keywords
 Evolutionary dynamics
 Developmental constraints
 Genetic constraints
 Lifehistory theory
 Matrix population models
 Adaptive dynamics
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SOCIOCOMPLEXITY  New Paradigms: H2020 ERC Consolidator Grant 2017
1/05/18 → 30/04/24
Project: Standard

Bringing the EES to the Classroom: Bringing the EES to the Classroom
1/09/19 → 31/05/21
Project: Standard