Abstract
BackgroundA fundamental and enduring problem in evolutionary biology is to understand how populations differentiate in the wild, yet little is known about what role organismal development plays in this process. Organismal development integrates environmental inputs with the action of gene regulatory networks to generate the phenotype. Core developmental gene networks have been highly conserved for millions of years across all animals, and therefore, organismal development may bias variation available for selection to work on. Biased variation may facilitate repeatable phenotypic responses when exposed to similar environmental inputs and ecological changes. To gain a more complete understanding of population differentiation in the wild, we integrated evolutionary developmental biology with population genetics, morphology, paleoecology and ecology. This integration was made possible by studying how populations of the ant species Monomorium emersoni respond to climatic and ecological changes across five ‘Sky Islands’ in Arizona, which are mountain ranges separated by vast ‘seas’ of desert. Sky Islands represent a replicated natural experiment allowing us to determine how repeatable is the response of M. emersoni populations to climate and ecological changes at the phenotypic, developmental, and gene network levels.ResultsWe show that a core developmental gene network and its phenotype has kept pace with ecological and climate change on each Sky Island over the last ∼90,000 years before present (BP). This response has produced two types of evolutionary change within an ant species: one type is unpredictable and contingent on the pattern of isolation of Sky lsland populations by climate warming, resulting in slight changes in gene expression, organ growth, and morphology. The other type is predictable and deterministic, resulting in the repeated evolution of a novel wingless queen phenotype and its underlying gene network in response to habitat changes induced by climate warming.ConclusionOur findings reveal dynamics of developmental gene network evolution in wild populations. This holds important implications: (1) for understanding how phenotypic novelty is generated in the wild; (2) for providing a possible bridge between micro- and macroevolution; and (3) for understanding how development mediates the response of organisms to past, and potentially, future climate change.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0448-4) contains supplementary material, which is available to authorized users.
Highlights
A fundamental and enduring problem in evolutionary biology is to understand how populations differentiate in the wild, yet little is known about what role organismal development plays in this process
This suggests that individuals in colonies of M. emersoni have adapted to local temperature conditions along the ecological gradients
A first split between southern (Huachucas and Chiricahuas) and northern (Pinaleños, Catalinas, and Pinals, Fig 1e and 3a) Sky Islands occurred around 80,000 years before present (BP) and was followed by the complete isolation of the 5 mountain ranges between 20,000 and 10,000 years BP (Additional file 1: Table S5, Figure S1 and S2). These results indicate that some Sky Island populations share a more recent history than others, but were subsequently isolated from one another during climatic warming
Summary
A fundamental and enduring problem in evolutionary biology is to understand how populations differentiate in the wild, yet little is known about what role organismal development plays in this process. Organismal development integrates the action of gene regulatory networks with environmental inputs to generate the phenotype [3, 17,18,19], and may play a key role in facilitating phenotypic differentiation of populations and species exposed to ecological changes [3, 17, 19]. The high degree of conservation and structure of developmental networks suggests that these networks may bias the variation that selection can act upon Such bias may facilitate repeatable phenotypic responses when populations are exposed to similar environmental inputs or encounter similar ecological changes [1, 3, 22, 23]. We use an integrative approach that combines multiple levels of organization (gene networks, development, and phenotype) as well as multiple fields (population genetics, paleoecology and ecology, morphology, and evolutionary developmental biology) to gain a more complete understanding of population differentiation in the wild
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