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Microevolutionary support for a developmental hourglass: gene expression patterns shape sequence variation and divergence in Drosophila
Author(s) -
Cruickshank Tami,
Wade Michael J.
Publication year - 2008
Publication title -
evolution and development
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 0.651
H-Index - 78
eISSN - 1525-142X
pISSN - 1520-541X
DOI - 10.1111/j.1525-142x.2008.00273.x
Subject(s) - biology , evolutionary biology , hourglass , gene , evolutionary developmental biology , genetics , human evolutionary genetics , phylogenetics , archaeology , history
SUMMARY A central goal of evolutionary developmental biology (Evo‐Devo) is to synthesize comparative molecular developmental genetics and its description of the dynamic relationship between genotype and phenotype with the microevolutionary processes (mutation, random drift, and selection) of population genetics. To this end, we analyzed sequence variation of five gene classes that act sequentially to shape early embryo development in Drosophila : maternal, gap, pair‐rule, segment polarity, and segment identity genes. We found two related patterns: (1) a microevolutionary pattern, wherein relative sequence variation within species is 2‐ to 3‐fold higher for maternal‐effect genes than for any other gene class; and, (2) a macroevolutionary pattern, wherein the relative sequence divergence among species for maternal‐effect genes is 2‐ to 4‐fold greater than for any other gene class. Both patterns are qualitatively and quantitatively consistent with the predictions of microevolutionary theory. Our findings connect within‐species genetic variation to between‐species divergence and shed light on the controversy over the existence of a “developmental hourglass,” where mid‐embryonic stages are more evolutionarily constrained than either earlier or later stages. Because maternal‐effect genes experience relaxed selective constraint relative to zygotic‐effect genes, they explore a wider mutational and phenotypic space. As a result, early acting maternal‐effect genes diverge more widely across taxa and thereby broaden the base of the developmental hourglass. In contrast, later acting zygotic genes are relatively more constrained and limited in their diversification across taxa, narrowing the waist of the developmental hourglass. This pattern is obscured by genes with both maternal and zygotic expression, which experience the strongest evolutionary constraint.