Biology subjects

Armisen, D.

Publications and source records attributed to Armisen, D..

10 recordsLinked to original sources

bioRxiv2024

The Fat/Hippo pathway drives photoperiod-induced wing length polyphenism

Identifying the genetic mechanisms that translate information from the environment into developmental programs to control size, shape and color are important for gaining insights into adaptation to changing environments. Insect polyphenisms provide good models to study such mechanisms because environmental factors are the main source of trait variation. Here we studied the genetic mechanism that controls photoperiod-induced wing length polyphenism in the water strider Gerris buenoi. By sequencing RNA sampled from wing buds across developmental stages under different photoperiodic conditions known to trigger alternative wing developmental trajectories, we found that differences in transcriptional activity arose primarily in the late 5th instar stage. Among the differentially expressed genes, the Fat/Hippo and ecdysone signaling pathways, both putative growth regulatory mechanisms showed significant enrichment. We used RNA interference against the differentially expressed genes Fat, Dachsous and Yorkie to assess whether they play a causative role in photoperiod induced wing length variation in Gerris buenoi. Our results show that the conserved Fat/Hippo pathway is a key regulatory network involved in the control of wing polyphenism in this species. This study provides an important basis for future comparative studies on the evolution of wing polyphenism and significantly deepens our understanding of the genetic regulation of insect polyphenisms.

evolutionary biology↗

bioRxiv2024

A shared genetic basis for sexually antagonistic male and female adaptations in the toothed water strider

Sexual conflict can drive the divergence of male and female phenotypes and several cross-species comparative analyses have documented patterns of correlated evolution of sex-specific traits that promote the evolutionary interests of the sexes. However, male-female coevolution can be highly dynamic. Moreover, if male and female traits do not have an entirely distinct genetic basis, this can have profound effects on their coevolutionary dynamics. Here, we use water striders, a well-studied model system for sexually antagonistic coevolution, and ask whether sex-specific phenotypic adaptations covary across populations and whether they share a common developmental genetic basis. Using comparative analyses both at the population and species levels, we document an association between a derived male mate-grasping trait and a likely female anti-grasping counteradaptation in the toothed water strider Gerris odontogaster. Interestingly, in one population where males did not express their derived grasping trait, females had also regained the ancestral morphology. We then used experimental manipulation of gene expression, and show that these male and female traits are both linked to a common developmental genetic program containing Hox and sex determination genes, despite the fact that they are different structures on different segments. Our work thus suggests that the pleiotropic nature of developmental genetic programs can blur the distinction between inter- and intralocus genetic conflict.

evolutionary biology↗

bioRxiv2024

A single giant cell at the origin of an evolutionary innovation

Key innovations play a central role in the diversification of lineages, yet our understanding of the mechanisms underlying their emergence remains fragmented. The propelling fan is a key innovation associated with the diversification of Rhagovelia water striders into fast flowing streams. Here, we show that a single giant cell is responsible for the development of the fan throughout embryogenesis. RNA interference against the fan-specific gene family gsha/mogsha depleted the fan in the embryo but did not alter the giant cell, indicating that these genes are not required for specifying the identity of this cell. gsha/mogsha instead seem to activate the expression of cuticular genes during early development, suggesting a role of these genes in regulating the accumulation of fan structural proteins. We also show that Hox genes act to block the giant cell in the fore- and rear-legs, thus restricting its fate to the mid-legs - the pair of legs that generates movement on water. In addition, Hox expression is specifically excluded from the giant cell, thus allowing the expression of the fans developmental genetic program. This study reveals that a single cell can be sufficient to generate innovative traits that have been central for a lineage to acquire new ecological opportunities and burst into diversification. One-sentence summaryA single giant cell orchestrates the developmental genetic program of a key innovation

evolutionary biology↗

bioRxiv2022

Modest transcriptomic response to polyploidization in allohexaploid wheat synthetics

Bread wheat is a recent allohexaploid (genomic constitution AABBDD) that emerged through a hybridization between tetraploid Triticum turgidum (AABB) and diploid Aegilops tauschii (DD) <10,000 years ago. The hexaploidization can be re-created artificially, producing synthetic wheat that has been used to study immediate genomic responses to polyploidization. Here we produced several synthetic wheats from alternative parental genotypes and reciprocal crosses, and examined transcriptomes from two different tissues and successive generations. We did not detect a massive reprogramming in gene expression, with only [~]1% of expressed genes showing significant differences compared to their lower-ploidy parents. Most of the differential expression is located on the D subgenome, without consistency in the direction of the expression change. Leaves and developing endosperm show distinct patterns of homoeologous expression bias, and almost non-overlapping sets of differentially expressed genes, implying that the polyploidization-triggered reprogramming is not effectuated through permanent (epi)genetic changes. While 0-3 families of transposable elements (TEs) became upregulated in wheat synthetics, we did not detect any significant association between TEs and the expression of nearby genes. We conclude that the modest tissue-specific and partially genotype-specific transcriptomic response to polyploidization is likely caused by rare incompatibilities of parental regulomes, and we discuss the pitfalls of transcriptomic comparisons across ploidy levels that can inflate the de-regulation signal.

genomics↗

bioRxiv2022

Transcriptome-based phylogeny of the semi-aquatic bugs (Hemiptera: Heteroptera: Gerromorpha) reveals patterns of lineage expansion in a series of new adaptive zones

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, they have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. The monophyletic group of water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a group of insects that transited to live on the water-air interface and diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones, representing distinct niches of water surfaces, and further diversification of the group. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

evolutionary biology↗

bioRxiv2020

Pleiotropy promotes male exaggerated weapon and its associated fighting behaviour in a water strider

Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body 1-3. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented 4,5. Here we show that the hyperallometric legs in the males of the water strider Microvelia longipes are associated with a specific signature of gene expression during development. Using RNAi knockdown, we demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric coefficient and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope in females. Furthermore, our data show that a tissue specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Overall, we demonstrate a genetic correlation between male body size, the exaggerated weapon, and the intense fighting behaviour associated with it in M. longipes. Our results provide evidence for a role of pleiotropy in the evolution of allometric slope.

evolutionary biology↗

bioRxiv2020

Impact of trait exaggeration on sex-biased gene expression and genome architecture in a water strider

Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of sex-specific phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the lack of a representative genome and transcriptomes to study the development of secondary sexual traits. Here we present the genome and developmental transcriptomes, focused on the legs of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs used as weapons. The quality of the genome assembly is such that over 90% of the sequence is captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in sex-biased genes, indicating a specific signature of gene expression in association with sex-specific trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. Interestingly, we found that female-biased genes that are expressed in the third legs only, but not male-biased genes, were over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed that they can arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Our findings shed light on how directional sexual selection drives sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

genomics↗

bioRxiv2018

Escalation and constraints of antagonistic armaments in water striders

Sexual conflict may result in the escalating coevolution of sexually antagonistic traits. However, our understanding of the evolutionary dynamics of antagonistic traits and their role in association with sex-specific escalation remains limited. Here we study sexually antagonistic coevolution in a genus of water striders called Rhagovelia. We identified a set of male grasping traits and female anti-grasping traits used during pre-mating struggles and show that natural variation of these traits is associated with variation in mating performance in the direction expected for antagonistic co-evolution. Phylogenetic mapping detected signals of escalation of these sexually antagonistic traits suggesting an ongoing arms race. Moreover, their escalation appears to be constrained by a trade-off with dispersal through flight in both sexes. Altogether our results highlight how sexual interactions may have shaped sex-specific antagonistic traits and how constraints imposed by natural selection may have influenced their evolution.

evolutionary biology↗

bioRxiv2018

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

genomics↗

bioRxiv2017

Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome

BackgroundThe Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae.\n\nResultsThe 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid-nutrition feeding.\n\nConclusionsWith the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus's strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes.

genomics↗