Phenotypic Innovation Research Articles

Morphological innovation and the evolution of hadrosaurid dinosaurs

AbstractThe hadrosaurids were a successful group of herbivorous dinosaurs. During the Late Cretaceous, 100 to 66 million years ago, hadrosaurids had high diversity, rapid speciation rates, and wide geographic distribution. Most hadrosaurids were large bodied and had similar postcranial skeletons. However, they show important innovations in the skull, including disparate crests that functioned as socio-sexual display structures, and a complex feeding apparatus, with specialized jaws bearing dental batteries. Little is known about the macroevolutionary processes that produced these evolutionary novelties. Here we provide novel perspectives using evolutionary rate and disparity analyses. Our results show that hadrosaurid cranial evolution was complex and dynamic, but their postcranial skeleton and body size were conservative. High cranial disparity was achieved through multiple bursts of phenotypic innovation. We highlight contrasting evolutionary trends within hadrosaurids between the disparate facial skeleton and crests, which both showed multiple high-rate shifts, and the feeding apparatus, which had low variance and high rates on a single phylogenetic branch leading to the diverse Saurolophidae. We reveal that rapid evolutionary rates were important for producing the high disparity of exaggerated crests and present novel evidence that the hadrosaurid diversification was linked to both a key adaptive innovation in the feeding apparatus and multiple bursts of innovation in socio-sexual displays.

Each of 3,323 metabolic innovations in the evolution of E. coli arose through the horizontal transfer of a single DNA segment

Even closely related prokaryotes often show an astounding diversity in their ability to grow in different nutritional environments. It has been hypothesized that complex metabolic adaptations-those requiring the independent acquisition of multiple new genes-can evolve via selectively neutral intermediates. However, it is unclear whether this neutral exploration of phenotype space occurs in nature, or what fraction of metabolic adaptations is indeed complex. Here, we reconstruct metabolic models for the ancestors of a phylogeny of 53 Escherichia coli strains, linking genotypes to phenotypes on a genome-wide, macroevolutionary scale. Based on the ancestral and extant metabolic models, we identify 3,323 phenotypic innovations in the history of the E. coli clade that arose through changes in accessory genome content. Of these innovations, 1,998 allow growth in previously inaccessible environments, while 1,325 increase biomass yield. Strikingly, every observed innovation arose through the horizontal acquisition of a single DNA segment less than 30 kb long. Although we found no evidence for the contribution of selectively neutral processes, 10.6% of metabolic innovations were facilitated by horizontal gene transfers on earlier phylogenetic branches, consistent with a stepwise adaptation to successive environments. Ninety-eight percent of metabolic phenotypes accessible to the combined E. coli pangenome can be bestowed on any individual strain by transferring a single DNA segment from one of the extant strains. These results demonstrate an amazing ability of the E. coli lineage to adapt to novel environments through single horizontal gene transfers (followed by regulatory adaptations), an ability likely mirrored in other clades of generalist bacteria.

Delayed trait development and the convergent evolution of shell kinesis in turtles.

Understanding developmental processes is foundational to clarifying the mechanisms by which convergent evolution occurs. Here, we show how a key convergently evolving trait is slowly 'acquired' in growing turtles. Many functionally relevant traits emerge late in turtle ontogeny, owing to design constraints imposed by the shell. We investigated this trend by examining derived patterns of shell formation associated with the multiple (at least 8) origins of shell kinesis in small-bodied turtles. Using box turtles as a model, we demonstrate that the flexible hinge joint required for shell kinesis differentiates gradually and via extensive repatterning of shell tissue. Disproportionate changes in shell shape and size substantiate that this transformation is a delayed ontogenetic response (3-5 years post-hatching) to structural alterations that arise in embryogenesis. These findings exemplify that the translation of genotype to phenotype may reach far beyond embryonic life stages. Thus, the temporal scope for developmental origins of adaptive morphological change might be broader than generally understood. We propose that delayed trait differentiation via tissue repatterning might facilitate phenotypic diversification and innovation that otherwise would not arise due to developmental constraints.

Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation.

Species-specific, new, or “orphan” genes account for 10%–30% of eukaryotic genomes. Although initially considered to have limited function, an increasing number of orphan genes have been shown to provide important phenotypic innovation. How new genes acquire regulatory sequences for proper temporal and spatial expression is unknown. Orphan gene regulation may rely in part on origination in open chromatin adjacent to preexisting promoters, although this has not yet been assessed by genome-wide analysis of chromatin states. Here, we combine taxon-rich nematode phylogenies with Iso-Seq, RNA-seq, ChIP-seq, and ATAC-seq to identify the gene structure and epigenetic signature of orphan genes in the satellite model nematode Pristionchus pacificus. Consistent with previous findings, we find young genes are shorter, contain fewer exons, and are on average less strongly expressed than older genes. However, the subset of orphan genes that are expressed exhibit distinct chromatin states from similarly expressed conserved genes. Orphan gene transcription is determined by a lack of repressive histone modifications, confirming long-held hypotheses that open chromatin is important for new gene formation. Yet orphan gene start sites more closely resemble enhancers defined by H3K4me1, H3K27ac, and ATAC-seq peaks, in contrast to conserved genes that exhibit traditional promoters defined by H3K4me3 and H3K27ac. Although the majority of orphan genes are located on chromosome arms that contain high recombination rates and repressive histone marks, strongly expressed orphan genes are more randomly distributed. Our results support a model of new gene origination by rare integration into open chromatin near enhancers.

Copy number variation is associated with gene expression change in archaea.

Genomic instability, although frequently deleterious, is also an important mechanism for microbial adaptation to environmental change. Although widely studied in bacteria, in archaea the effect of genomic instability on organism phenotypes and fitness remains unclear. Here we use DNA segmentation methods to detect and quantify genome-wide copy number variation (CNV) in large compendia of high-throughput datasets in a model archaeal species, Halobacterium salinarum. CNV hotspots were identified throughout the genome. Some hotspots were strongly associated with changes in gene expression, suggesting a mechanism for phenotypic innovation. In contrast, CNV hotspots in other genomic loci left expression unchanged, suggesting buffering of certain phenotypes. The correspondence of CNVs with gene expression was validated with strain- and condition-matched transcriptomics and DNA quantification experiments at specific loci. Significant correlation of CNV hotspot locations with the positions of known insertion sequence (IS) elements suggested a mechanism for generating genomic instability. Given the efficient recombination capabilities in H. salinarum despite stability at the single nucleotide level, these results suggest that genomic plasticity mediated by IS element activity can provide a source of phenotypic innovation in extreme environments.

Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera

The importance of gene duplication in developmental body plan evolution is well established, but for many megadiverse clades such as true flies (Diptera), a comprehensive understanding is still just emerging through comparative genomics. In a survey of 377 developmental gene families, we found that in addition to the pea aphid, which has been previously shown to be genome-wide enriched with gene duplicates and was included as positive control, more than twice as many expanded developmental gene families were observed in Drosophila (49) compared to mosquito (21), flour beetle (20), and honey bee (14). Synonymous sequence divergence estimates and ortholog conservation analyses in additional dipteran genomes revealed that most Drosophila gene duplicates are ancient and accumulated during a time window that reaches back to the origin of brachyceran flies, approximately 180 million years ago. Further, available genetic data suggest that more than half of the Drosophila developmental gene duplicates remained partially or even fully redundant despite their ancient separation. We therefore speculate that the exceptional accumulation of developmental gene duplicates in Drosophila and the higher Diptera was proximally driven by the evolution of fast development, benefiting from increased genetic robustness. At the same time, the concomitant increase of opportunities for gene duplicate diversification appears to have been a source for developmental and phenotypic innovation during the unparalleled diversification of brachyceran Diptera.

MIPhy: identify and quantify rapidly evolving members of large gene families.

After transitioning to a new environment, species often exhibit rapid phenotypic innovation. One of the fastest mechanisms for this is duplication followed by specialization of existing genes. When this happens to a member of a gene family, it tends to leave a detectable phylogenetic signature of lineage-specific expansions and contractions. These can be identified by analyzing the gene family across several species and identifying patterns of gene duplication and loss that do not correlate with the known relationships between those species. This signature, termed phylogenetic instability, has been previously linked to adaptations that change the way an organism samples and responds to its environment; conversely, low phylogenetic instability has been previously linked to proteins with endogenous functions. With the increase in genome-level data, there is a need to identify and quantify phylogenetic instability. Here, we present Minimizing Instability in Phylogenetics (MIPhy), a tool that solves this problem by quantifying the incongruence of a gene’s evolutionary history. The motivation behind MIPhy was to produce a tool to aid in interpreting phylogenetic trees. It can predict which members of a gene family are under adaptive evolution, working only from a gene tree and the relationship between the species under consideration. While it does not conduct any estimation of positive selection—which is the typical indication of adaptive evolution—the results tend to agree. We demonstrate the usefulness of MIPhy by accurately predicting which members of the mammalian cytochrome P450 gene superfamily metabolize xenobiotics and which metabolize endogenous compounds. Our predictions correlate very well with known substrate specificities of the human enzymes. We also analyze the Caenorhabditis collagen gene family and use MIPhy to predict genes that produce an observable phenotype when knocked down in C. elegans, and show that our predictions correlate well with existing knowledge. The software can be downloaded and installed from https://github.com/dave-the-scientist/miphy and is also available as an online web tool at http://www.miphy.wasmuthlab.org.

The evolution of the tetrapod humerus: morphometrics, disparity, and evolutionary rates

ABSTRACTThe present study explores the macroevolutionary dynamics of shape changes in the humeri of all major grades and clades of early tetrapods and their fish-like forerunners. Coordinate point eigenshape analysis applied to humeral outlines in extensor view reveals that fish humeri are more disparate than those of most early tetrapod groups and significantly separate from the latter. Our findings indicate sustained changes in humeral shape in the deepest portions of the tetrapod stem group and certain portions of the crown. In the first half of sampled tetrapod history, subclades show larger than expected humeral disparity, suggesting rapid diffusion into morphospace. Later in tetrapod evolution, subclades occupy smaller and non-overlapping morphospace regions. This pattern may reflect in part increasing specialisations in later tetrapod lineages. Bayesian shifts in rates of evolutionary change are distributed discontinuously across the phylogeny, and most of them occur within rather than between major groups. Most shifts with the highest Bayesian posterior probabilities are observed in lepospondyls. Similarly, maximum likelihood analyses of shifts support marked rate accelerations in lepospondyls and in various subclades within that group. In other tetrapod groups, rates either tend to slow down or experience only small increases. Somewhat surprisingly, no shifts are concurrent with structural, functional, or ecological innovations in tetrapod evolution, including the origin of digits, the water–land transition and increasing terrestrialisation. Although counterintuitive, these results are consistent with a model of continual phenotypic innovation that, although decoupled from key evolutionary changes, is possibly triggered by niche segregation in divergent clades and grades of early tetrapods.

The Divergent Genomes of Teleosts.

Boasting nearly 30,000 species, teleosts account for half of all extant vertebrates and approximately 98% of all ray-finned fish species (Actinopterygii). Teleosts are also the largest and most diverse group of vertebrates, exhibiting an astonishing level of morphological, physiological, and behavioral diversity. Previous studies had indicated that the teleost lineage has experienced an additional whole-genome duplication event. Recent comparative genomic analyses of teleosts and other bony vertebrates using spotted gar (a nonteleost ray-finned fish) and elephant shark (a cartilaginous fish) as outgroups have revealed several divergent features of teleost genomes. These include an accelerated evolutionary rate of protein-coding and nucleotide sequences, a higher rate of intron turnover, loss of many potential cis-regulatory elements and shorter conserved syntenic blocks. A combination of these divergent genomic features might have contributed to the evolution of the amazing phenotypic diversity and morphological innovations of teleosts.

A Molecular Portrait of De Novo Genes in Yeasts

New genes, with novel protein functions, can evolve "from scratch" out of intergenic sequences. These de novo genes can integrate the cell's genetic network and drive important phenotypic innovations. Therefore, identifying de novo genes and understanding how the transition from noncoding to coding occurs are key problems in evolutionary biology. However, identifying de novo genes is a difficult task, hampered by the presence of remote homologs, fast evolving sequences and erroneously annotated protein coding genes. To overcome these limitations, we developed a procedure that handles the usual pitfalls in de novo gene identification and predicted the emergence of 703 de novo gene candidates in 15 yeast species from 2 genera whose phylogeny spans at least 100 million years of evolution. We validated 85 candidates by proteomic data, providing new translation evidence for 25 of them through mass spectrometry experiments. We also unambiguously identified the mutations that enabled the transition from noncoding to coding for 30 Saccharomyces de novo genes. We established that de novo gene origination is a widespread phenomenon in yeasts, only a few being ultimately maintained by selection. We also found that de novo genes preferentially emerge next to divergent promoters in GC-rich intergenic regions where the probability of finding a fortuitous and transcribed ORF is the highest. Finally, we found a more than 3-fold enrichment of de novo genes at recombination hot spots, which are GC-rich and nucleosome-free regions, suggesting that meiotic recombination contributes to de novo gene emergence in yeasts.

Phenotypic Innovation and Adaptive Constraints in the Evolutionary Radiation of Palaeozoic Crinoids

To better understand the patterns and processes shaping large-scale phenotypic diversification, I integrate palaeobiological and phylogenetic perspectives to investigate a ~200-million-year radiation using a global sample of Palaeozoic crinoid echinoderms. Results indicate the early history of crinoid diversification is characterized by early burst dynamics with decelerating morphologic rates. However, in contrast with expectation for a single “early burst” model, morphospace continued to expand following a slowdown in rates. In addition, I find evidence for an isolated peak in morphologic rates occurring late in the clade’s history. This episode of elevated rates is not associated with increased disparity, morphologic novelty, or the radiation of a single subclade. Instead, this episode of elevated rates involved multiple subclade radiations driven by environmental change toward a pre-existing adaptive optimum. The decoupling of morphologic disparity with rates of change suggests phenotypic rates are primarily shaped by ecologic factors rather than the origination of morphologic novelty alone. These results suggest phenotypic diversification is far more complex than models commonly assumed in comparative biology. Furthermore, palaeontological disparity patterns are not a reliable proxy for rates after an initial diversifying phase. These issues highlight the need for continued synthesis between fossil and phylogenetic approaches to macroevolution.

Genetic Basis of Exploiting Ecological Opportunity During the Long-Term Diversification of a Bacterial Population.

Adaptive diversification is an essential evolutionary process, one that produces phenotypic innovations including the colonization of available ecological niches. Bacteria can diverge in sympatry when ecological opportunities allow, but the underlying genetic mechanisms are often unknown. Perhaps, the longest-lasting adaptive diversification seen in the laboratory occurred during the long-term evolution experiment, in which 12 populations of Escherichia coli have been evolving independently for more than 65,000 generations from a common ancestor. In one population, two lineages, S and L, emerged at ~6500 generations and have dynamically coexisted ever since by negative frequency-dependent interactions mediated, in part, by acetate secretion by L. Mutations in spoT, arcA, and gntR promoted the emergence of the S lineage, although they reproduced only partially its phenotypic traits. Here, we characterize the evolved mechanism of acetate consumption by the S lineage that enabled invasion and coexistence with the L lineage. We identified an additional mutation in acs that, together with the arcA mutation, drove an early restructuring of the transcriptional control of central metabolism in S, leading to improved acetate consumption. Pervasive epistatic interactions within the S genome contributed to the exploitation of this new ecological opportunity. The emergence and maintenance of this long-term polymorphism is a complex multi-step process.

Extending epigenesis: from phenotypic plasticity to the bio-cultural feedback

The paper aims at proposing an extended notion of epigenesis acknowledging an actual causal import to the phenotypic dimension for the evolutionary diversification of life forms. “Introductory remarks” section offers introductory remarks on the issue of epigenesis contrasting it with ancient and modern preformationist views. In “Transmutation of forms: phenotypic variation, diversification, and complexification” section we propose to intend epigenesis as a process of phenotypic formation and diversification (a) dependent on environmental influences, (b) independent of changes in the genomic nucleotide sequence, and (c) occurring during the whole life span. Then, “Evolvability and phenotypic evolution” section focuses on phenotypic plasticity and offers an overview of basic properties (like robustness, modularity and degeneracy) that allows biological systems to be evolvable—i.e. to have the potentiality of producing phenotypic variation. Successively (“Environmental induction of phenotypic changes” section), the emphasis is put on environmentally-induced modifications in the regulation of gene expression giving rise to phenotypic variation and diversification. After some brief considerations on the debated issue of epigenetic inheritance (“Assessing epigenetic inheritance” section), the issue of culture (kept in the background of the preceding sections) is considered. The key point is that, in the case of humans and of the evolutionary history of the genus Homo at least, the environment is also, importantly, the cultural environment. Thus, “Bio-cultural feedback” section argues that a bio-cultural feedback should be acknowledged in the “epigenic” processes leading to phenotypic diversification and innovation in Homo evolution. Finally, “Brain plasticity and cultural neural reuse” section introduces the notion of “cultural neural reuse”, which refers to phenotypic/neural modifications induced by specific features of the cultural environment that are effective in human cultural evolution without involving genetic changes. Therefore, cultural neural reuse may be regarded as a key instance of the bio-cultural feedback and ultimately of the extended notion of epigenesis proposed in this work.

Single Cell Transcriptomics, Mega-Phylogeny, and the Genetic Basis of Morphological Innovations in Rhizaria.

The innovation of the eukaryote cytoskeleton enabled phagocytosis, intracellular transport, and cytokinesis, and is largely responsible for the diversity of morphologies among eukaryotes. Still, the relationship between phenotypic innovations in the cytoskeleton and their underlying genotype is poorly understood. To explore the genetic mechanism of morphological evolution of the eukaryotic cytoskeleton, we provide the first single cell transcriptomes from uncultured, free-living unicellular eukaryotes: the polycystine radiolarian Lithomelissa setosa (Nassellaria) and Sticholonche zanclea (Taxopodida). A phylogenomic approach using 255 genes finds Radiolaria and Foraminifera as separate monophyletic groups (together as Retaria), while Cercozoa is shown to be paraphyletic where Endomyxa is sister to Retaria. Analysis of the genetic components of the cytoskeleton and mapping of the evolution of these on the revised phylogeny of Rhizaria reveal lineage-specific gene duplications and neofunctionalization of α and β tubulin in Retaria, actin in Retaria and Endomyxa, and Arp2/3 complex genes in Chlorarachniophyta. We show how genetic innovations have shaped cytoskeletal structures in Rhizaria, and how single cell transcriptomics can be applied for resolving deep phylogenies and studying gene evolution in uncultured protist species.

A set of genes conserved in sequence and expression traces back the establishment of multicellularity in social amoebae.

BackgroundThe developmental cycle of Dictyostelid amoebae represents an early form of multicellularity with cell type differentiation. Mutant studies in the model Dictyostelium discoideum revealed that its developmental program integrates the actions of genes involved in signal transduction, adhesion, motility, autophagy and cell wall and matrix biosynthesis. However, due to functional redundancy and fail safe options not required in the laboratory, this single organism approach cannot capture all essential genes.To understand how multicellular organisms evolved, it is essential to recognize both the conserved core features of their developmental programs and the gene modifications that instigated phenotypic innovation. For complex organisms, such as animals, this is not within easy reach, but it is feasible for less complex forms, such as the Dictyostelid social amoebas.ResultsWe compared global profiles of gene expression during the development of four social amoebae species that represent 600 mya of Dictyostelia evolution, and identified orthologous conserved genes with similar developmental up-regulation of expression using three different methods. For validation, we disrupted five genes of this core set and examined the phenotypic consequences.ConclusionAt least 71 of the developmentally regulated genes that were identified with all methods were likely to be already present in the last ancestor of all Dictyostelia. The lack of phenotypic changes in null mutants indicates that even highly conserved genes either participate in functionally redundant pathways or are necessary for developmental progression under adverse, non-standard laboratory conditions. Both mechanisms provide robustness to the developmental program, but impose a limit on the information that can be obtained from deleting single genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3223-z) contains supplementary material, which is available to authorized users.

Phenotypic innovation through recombination in genome-scale metabolic networks.

Recombination is an important source of metabolic innovation, especially in prokaryotes, which have evolved the ability to survive on many different sources of chemical elements and energy. Metabolic systems have a well-understood genotype-phenotype relationship, which permits a quantitative and biochemically principled understanding of how recombination creates novel phenotypes. Here, we investigate the power of recombination to create genome-scale metabolic reaction networks that enable an organism to survive in new chemical environments. To this end, we use flux balance analysis, an experimentally validated computational method that can predict metabolic phenotypes from metabolic genotypes. We show that recombination is much more likely to create novel metabolic abilities than random changes in chemical reactions of a metabolic network. We also find that phenotypic innovation is more likely when recombination occurs between parents that are genetically closely related, phenotypically highly diverse, and viable on few rather than many carbon sources. Survival on a new carbon source preferentially involves reactions that are superessential, that is, essential in many metabolic networks. We validate our observations with data from 61 reconstructed prokaryotic metabolic networks. Our systematic and quantitative analysis of metabolic systems helps understand how recombination creates innovation.

Whole genome sequencing of a banana wild relative Musa itinerans provides insights into lineage-specific diversification of the Musa genus.

Crop wild relatives are valuable resources for future genetic improvement. Here, we report the de novo genome assembly of Musa itinerans, a disease-resistant wild banana relative in subtropical China. The assembled genome size was 462.1 Mb, covering 75.2% of the genome (615.2Mb) and containing 32, 456 predicted protein-coding genes. Since the approximate divergence around 5.8 million years ago, the genomes of Musa itinerans and Musa acuminata have shown conserved collinearity. Gene family expansions and contractions enrichment analysis revealed that some pathways were associated with phenotypic or physiological innovations. These include a transition from wood to herbaceous in the ancestral Musaceae, intensification of cold and drought tolerances, and reduced diseases resistance genes for subtropical marginally distributed Musa species. Prevalent purifying selection and transposed duplications were found to facilitate the diversification of NBS-encoding gene families for two Musa species. The population genome history analysis of M. itinerans revealed that the fluctuated population sizes were caused by the Pleistocene climate oscillations, and that the formation of Qiongzhou Strait might facilitate the population downsizing on the isolated Hainan Island about 10.3 Kya. The qualified assembly of the M. itinerans genome provides deep insights into the lineage-specific diversification and also valuable resources for future banana breeding.

Evolution of Genome Size in Asexual Digital Organisms.

Genome sizes have evolved to vary widely, from 250 bases in viroids to 670 billion bases in some amoebas. This remarkable variation in genome size is the outcome of complex interactions between various evolutionary factors such as mutation rate and population size. While comparative genomics has uncovered how some of these evolutionary factors influence genome size, we still do not understand what drives genome size evolution. Specifically, it is not clear how the primordial mutational processes of base substitutions, insertions, and deletions influence genome size evolution in asexual organisms. Here, we use digital evolution to investigate genome size evolution by tracking genome edits and their fitness effects in real time. In agreement with empirical data, we find that mutation rate is inversely correlated with genome size in asexual populations. We show that at low point mutation rate, insertions are significantly more beneficial than deletions, driving genome expansion and the acquisition of phenotypic complexity. Conversely, the high mutational load experienced at high mutation rates inhibits genome growth, forcing the genomes to compress their genetic information. Our analyses suggest that the inverse relationship between mutation rate and genome size is a result of the tradeoff between evolving phenotypic innovation and limiting the mutational load.Supplementary informationThe online version of this article (doi:10.1038/srep25786) contains supplementary material, which is available to authorized users.

CDROM: Classification of Duplicate gene RetentiOn Mechanisms.

BackgroundGene duplication is a major source of new genes that is thought to play an important role in phenotypic innovation. Though several mechanisms have been hypothesized to drive the functional evolution and long-term retention of duplicate genes, there are currently no software tools for assessing their genome-wide contributions. Thus, the evolutionary mechanisms by which duplicate genes acquire novel functions remain unclear in a number of taxa.ResultsIn a recent study, researchers developed a phylogenetic approach that uses gene expression data from two species to classify the mechanisms underlying the retention of duplicate genes (Proc Natl Acad Sci USA 110:1740917414, 2013). We have implemented their classification method, as well as a more generalized method, in the R package CDROM, enabling users to apply these methods to their data and gain insights into the origin of novel biological functions after gene duplication. The CDROM R package, source code, and user manual for the R package are available for download from CRAN at https://cran.rstudio.com/web/packages/CDROM/. Additionally, the CDROM R source code, user manual for running CDROM from the source code, and sample dataset used in this manuscript can be accessed at www.personal.psu.edu/rua15/software.html.ConclusionsCDROM is the first software package that enables genome-wide classification of the mechanisms driving the long-term retention of duplicate genes. It is user-friendly and flexible, providing researchers with a tool for studying the functional evolution of duplicate genes in a variety of taxa.

Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants.

BackgroundReproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species.ResultsUsing queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their ‘eigengenes’. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another.ConclusionsThese results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0902-7) contains supplementary material, which is available to authorized users.