INDEHISCENT regulates explosive seed dispersal

How traits evolve to produce novelty or stasis is an open question in biology. We investigate this question in Cardamine hirsuta, a relative of Arabidopsis thaliana that employs explosive fracture to disperse its seeds. This trait evolved through key morphomechanical innovations that distinguish the otherwise very similar, dehiscent fruit of these two species. Using CRISPR/Cas9, we show that dehiscence zone formation is absolutely required for explosive fracture in C. hirsuta, and is controlled by the bHLH transcription factor INDEHISCENT (IND). Using mutant screens, we identified the MADS-box transcription factor FRUITFULL (FUL) as a negative regulator of IND in C. hirsuta. Although FUL function is conserved in C. hirsuta, the consequences of IND mis-expression differ in ful mutants of C. hirsuta versus A. thaliana. In ful mutants of both species, valve tissue is replaced by dehiscence zone tissue, which comprises two distinct cell types: lignified layer and separation layer cells. While A. thaliana ful mutants develop stunted fruit with ectopic lignified layer cells, C. hirsuta ful mutants have elongated fruit with ectopic separation layer cells. We show that IND dose determines the proportion of these two cell types in ectopic dehiscence zones. We also show that the extent of ectopic lignification caused by IND mis-expression determines fruit length. Our findings indicate developmental system drift in the conserved gene network patterning dehiscent fruit in two related Brassicaceae species.

Allopatric divergence limits cheating range and alters genetic requirements for a cooperative trait

Social and genomic context may constrain the fates of mutations in cooperation genes. While some mechanisms limiting cheaters evolve in the presence of cheating, here we ask whether cheater resistance can evolve latently even in environments where cooperation is not expressed and cheaters are absent. The bacterium Myxococcus xanthus undergoes cooperative multicellular development upon starvation, but developmentally defective cheaters can outcompete cooperators within mixed groups. Using natural isolates and an obligate cheater disrupted at the developmental-signaling gene csgA, we show that cheating range is narrow among natural strains due to antagonisms that do not specifically target cheaters. Further, we mixed the cheater with closely related cooperators that diverged from it allopatrically in nutrient-rich environments in which cooperative development does not occur, showing that even slight divergence under these conditions can eliminate cheating phenotypes. Our results suggest that such cooperation- and cheater-blind divergence can generate a geographic mosaic of local cheater-cooperator compatibility patches that limit cheater spread. We also ask whether genomic divergence can shape the fitness effects of disrupting a cooperation gene. Construction of the same csgA mutation in several natural-isolate cooperators generated a wide range of pure-culture sporulation phenotypes, from a complete defect to no defect. Thus, we find that epistatic interactions limit the range of genomes within which a mutation creates a cooperation defect. Moreover, these results reveal Developmental System Drift in a microbial system because sporulation proficiency is conserved across the natural isolates despite divergence in the role of csgA.

Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos

Ascidians with very similar embryos but highly divergent genomes are thought to have undergone extensive developmental system drift. We compared, in four species (Ciona and Phallusia for Phlebobranchia, Molgula and Halocynthia for Stolidobranchia), gene expression and gene regulation for a network of six transcription factors regulating peripheral nervous system (PNS) formation in Ciona. All genes, but one in Molgula, were expressed in the PNS with some differences correlating with phylogenetic distance. Cross-species transgenesis indicated strong levels of conservation, except in Molgula, in gene regulation despite lack of sequence conservation of the enhancers. Developmental system drift in ascidians is thus higher for gene regulation than for gene expression and is impacted not only by phylogenetic distance, but also in a clade-specific manner and unevenly within a network. Finally, considering that Molgula is divergent in our analyses, this suggests deep conservation of developmental mechanisms in ascidians after 390 My of separate evolution.

Functional evidence that Activin/Nodal signaling is required for establishing the dorsal-ventral axis in the annelid Capitella teleta

ABSTRACTThe TGF-β superfamily comprises two distinct branches: the Activin/Nodal and BMP pathways. During development, signaling by this superfamily regulates a variety of embryological processes, and it has a conserved role in patterning the dorsal-ventral body axis. Recent studies show that BMP signaling establishes the dorsal-ventral axis in some mollusks. However, previous pharmacological inhibition studies in the annelid Capitella teleta, a sister clade to the mollusks, suggests that the dorsal-ventral axis is patterned via Activin/Nodal signaling. Here, we determine the role of both the Activin/Nodal and BMP pathways as they function in Capitella axis patterning. Antisense morpholino oligonucleotides were targeted to Ct-Smad2/3 and Ct-Smad1/5/8, transcription factors specific to the Activin/Nodal and BMP pathways, respectively. Following microinjection of zygotes, resulting morphant larvae were scored for axial anomalies. We demonstrate that the Activin/Nodal pathway of the TGF-β superfamily, but not the BMP pathway, is the primary dorsal-ventral patterning signal in Capitella. These results demonstrate variation in the molecular control of axis patterning across spiralians, despite sharing a conserved cleavage program. We suggest that these findings represent an example of developmental system drift.

Speciation and the developmental alarm clock

New species arise as the genomes of populations diverge. The developmental ‘alarm clock’ of speciation sounds off when sufficient divergence in genetic control of development leads hybrid individuals to infertility or inviability, the world awoken to the dawn of new species with intrinsic post-zygotic reproductive isolation. Some developmental stages will be more prone to hybrid dysfunction due to how molecular evolution interacts with the ontogenetic timing of gene expression. Considering the ontogeny of hybrid incompatibilities provides a profitable connection between ‘evo-devo’ and speciation genetics to better link macroevolutionary pattern, microevolutionary process, and molecular mechanisms. Here, we explore speciation alongside development, emphasizing their mutual dependence on genetic network features, fitness landscapes, and developmental system drift. We assess models for how ontogenetic timing of reproductive isolation can be predictable. Experiments and theory within this synthetic perspective can help identify new rules of speciation as well as rules in the molecular evolution of development.

Speciation and the developmental alarm clock

New species arise as the genomes of populations diverge. The developmental ‘alarm clock’ of speciation sounds off when sufficient divergence in genetic control of development leads hybrid individuals to infertility or inviability, the world awoken to the dawn of new species with intrinsic post-zygotic reproductive isolation. Some developmental stages will be more prone to hybrid dysfunction due to how molecular evolution interacts with the ontogenetic timing of gene expression. Considering the ontogeny of hybrid incompatibilities provides a profitable connection between ‘evo-devo’ and speciation genetics to better link macroevolutionary pattern, microevolutionary process, and molecular mechanisms. Here we explore speciation alongside development, emphasizing their mutual dependence on genetic network features, fitness landscapes, and developmental system drift. We assess models for how ontogenetic timing of reproductive isolation can be predictable. Experiments and theory within this synthetic perspective can help identify new rules of speciation as well as rules in the molecular evolution of development.Impact StatementIntegrating speciation genetics with ontogeny can identify predictable rules in the molecular evolution of developmental pathways and in the accumulation of reproductive isolation as genomes diverge.

Comparison of developmental genome expression in rodent molars reveals extensive developmental system drift

In evolution, it is widely believed that phenotypic changes root in developmental changes and phenotype conservation, in developmental conservation. Seeming phenotype conservation may however hide evolutionary changes in the underlying developmental mechanisms by which a trait is produced. This cryptic evolution is also called Developmental System Drift, and the extent of this phenomenon unclear. We used a well-characterized evo-devo model system, rodent molars, to test the correlation between phenotypic and developmental evolution. Between mouse and hamster, the morphology of the lower molars has much less diverged than the morphology of the upper molars. Is development accordingly more conserved? We compared molar crown formation with a standard approach, and with a tight transcriptome time-series to get a quantitative molecular profiling of developmental states. Our data identify common trends in the development of all molars. Upper and lower molars have their specificities since the early steps of morphogenesis, at the levels of the pattern of cusp formation, cellular composition and biased gene expression. The extent of difference in lower vs. upper molar development within one species does correlate with the extent of difference in final morphology. However, the specificity of lower vs. upper molar development is drowned among the rapid evolution of development, which is highly species-specific in term of expression levels and temporal profiles. Divergence in developmental systems is almost as high for lower as it is for upper molar, despite much lesser morphological changes in lower molar crown. Hence, our results point an extensive drift in this developmental system. Because serial organs are largely sharing gene networks, it supports previous theoretical work that suggest a causal link between pleiotropy and DSD.