Past climate change on Sky Islands drives novelty in a core developmental gene network and its phenotype

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.

Interruption points in the wing gene regulatory network underlying wing polyphenism evolved independently in male and female morphs in Cardiocondyla ants

“…This suggests that in wingless female workers, wing‐disc precursor cells may separate from the leg disc precursor cells in the late embryo, migrate dorsally but stop further proliferation, as observed in Pheidole megacephala minor workers (Sameshima et al, ). This inference is further supported by the complete lack of expression of genes in the wing network in other species, where the workers lack visible rudimentary wing discs: the minor workers of Pheidole morrisi (Abouheif & Wray, ) and workers in Monomorium emersoni (Favé et al, ).…”

“…The expression patterns of three transcription factors ultrabithorax ( ubx) , extradenticle ( exd ), and cut ( ct ) were investigated in late‐third larval instar wing discs of C. obscurior using primary antibodies shown to cross‐react in ants (Abouheif & Wray, ; Favé et al, ). Based on the procedure of Patel (), dissected larvae of C. obscurior were rehydrated, washed several times in PTW (01% Tween 20 in PBS), and blocked for 2 hr with anti‐goat serum.…”

“…However, at the same time, this network is interrupted at specific points in the wingless worker caste (Nahmad, Glass, & Abouheif, ); some interruption points are similar, whereas other interruption points are different in wingless worker castes across different ant species (Abouheif & Wray, ; Bowsher, Wray, & Abouheif, ; Shbailat & Abouheif, ). Finally, several species have independently evolved winged and wingless queen castes that exhibit similar, as well as divergent interruption points (Favé et al, ; Belhagues et al, ). Taken together, this indicates that the gene network underlying wing polyphenism in ants has evolved in a mosaic fashion, where interruption of the expression of some genes is conserved, whereas interruption of other genes is evolutionary labile (Abouheif & Wray, ; Shbailat & Abouheif, ).…”

How mountains shape biodiversity: The role of the Andes in biogeography, diversification, and reproductive biology in South America's most species‐rich lizard radiation (Squamata: Liolaemidae)

“…Rapid mountain building creates a phenomenon known as “sky islands.” These islands provide ecological opportunity in new habitats devoid of competitors and therefore increase rates of speciation through allopatric isolation (Schluter ; Gavrilets and Vose ; Favé et al. ; Hazzi et al. ).…”

Lack of interruption of the gene network underlying wing polyphenism in an early‐branching ant genus

“…Our results also raise the possibility that wingless workers and wingless queens may have evolved through similar mechanisms and that the phylogenetic ladder pattern may also hold for wingless queens—the interruption points in wing GRN of wingless queens of the derived ant species Monomorium (Fave et al., ) appear to occur further upstream than in those of M. oberthueri (Figure ). However, unlike wingless workers, only a few genes and species have been sampled so far, and some exceptions to this trend may exist.…”