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Chipman, A. D.

Publications and source records attributed to Chipman, A. D..

8 recordsLinked to original sources

Gene family evolutionary dynamics reveal convergent genomic signatures in pancrustacean metamorphosis

Arthropod developmental modes are highly diverse, ranging from direct development with little morphological change between moults to metamorphic life-stage progressions characterised by profound transformations. Metamorphosis can be defined as a post-embryonic life-stage progression event leading to adulthood that is characterised by major morphological changes and modifications of the adaptive landscape. Within this framework, we compare four independent evolutionary life history transitions to metamorphic development across Pancrustacea. Using a phylogenomic dataset of 54 species spanning 26 orders, we investigated gene family evolutionary dynamics associated with the inferred origins of metamorphosis in Insecta, Copepoda, Eucarida, and Thecostraca. Compared with non-metamorphic sister lineages as well as descendent and ancestral nodes, transitions to metamorphic development were consistently associated with elevated gene family births and expansions. Although these expansions predominantly involved different gene families in each lineage, they repeatedly converged on shared biological functions, particularly those related to embryonic and post-embryonic development, morphogenesis, nervous system differentiation, and other processes relevant to the biology and evolution of metamorphosis. Evolutionary modelling further identified a subset of gene families exhibiting adaptive, lineage-specific expansions, including genes implicated in neural and sensory development, segmentation, and moulting. Together, these findings support a model in which independent transitions to metamorphic development repeatedly recruited different components of a shared developmental toolkit, achieving functional convergence through distinct genetic trajectories. This reframes the arthropod moulting programme as an evolutionarily flexible developmental substrate whose repeated modification has facilitated the emergence of complex multi-phasic life histories and contributed to the extraordinary diversification of Pancrustacea.

evolutionary biology↗

Moulting in Pancrustacea is characterised by both deeplyconserved and recently evolved gene modules

Arthropods such as insects and crustaceans, which together form the monophyletic group Pancrustacea, possess a rigid chitinous exoskeleton that must be periodically shed through moulting to allow growth and morphological change. Although moulting is a deeply conserved developmental process across Arthropoda, our understanding of its molecular mechanisms is still largely derived from insect model species. Lineage-specific innovations and losses of moulting related genes raise fundamental questions on the extent of its conservation outside non-insect arthropods. Here, we investigate the evolutionary conservation of moulting gene expression across five representative pancrustacean species using publicly available transcriptomic datasets. Changes in gene expression during moulting are characterized by both deeply conserved and lineage-specific gene modules. Temporal gene expression analyses reveal that these lineage-specific signatures are not uniformly distributed across the moulting process: the middle transitional phase is more lineage-specific, thereby exhibiting an inverse hourglass pattern. This is likely due to life-history specific processes, development of the cuticle and specialized structures of the exoskeleton. Overall, this study provides evidence for both the evolutionary conservation and divergence of this key post-embryonic developmental process and highlights the modular architecture of the moulting programme.

evolutionary biology↗

Evolutionary dynamics of the arthropod moulting machinery

Exoskeletons define arthropods, providing support for segmented bodies and appendages while protecting against environmental stress and predation. Although ubiquitous, this evolutionarily variable feature has enabled arthropods to occupy diverse lifestyles and ecological niches, contributing to their unrivalled diversity. Because the chitinous cuticle is rigid, exoskeletons must be periodically shed and replaced as animals grow. Arthropods therefore develop through discrete moults, with conserved phases that progress from pre-moult preparation to ecdysis and post-moult maturation. These are tightly regulated developmental transitions controlled by a molecular toolkit comprising neuropeptides, hormone-synthesising enzymes, receptors, and the early, fate, and late gene sets that activate and execute the moulting process. Although genetic studies in model species have identified many components, major knowledge gaps remain, especially in non-insect arthropods. Advances in genome sequencing now enable comparative genomic analyses across diverse, previously understudied arthropod lineages to begin to address these gaps. We present a comprehensive comparative genomic survey of arthropods, sampling all four subphyla: Chelicerata, Myriapoda, Crustacea, and Hexapoda. Orthology inference and gene copy-number analyses contrast stable and dynamic components of the moulting machinery across the phylum. Ancestral state reconstructions and phylogenetic reconciliations reveal gene duplication and loss dynamics and the evolutionary histories of key moulting gene families. The inclusion of newly generated myriapod genomes addresses a major taxonomic gap and enables inferences of gene repertoire changes in the Mandibulata ancestor. The broad taxonomic representation enables a phylum-wide assessment to systematically evaluate, refine, and revise current understanding of the evolutionary dynamics of the entire moulting genetic toolkit.

evolutionary biology↗

Early Embryonic Development of the German Cockroach Blattella germanica

BackgroundEarly embryogenesis is characterized by dramatic cell proliferation and movement. In most insects, early embryogenesis includes a phase called the uniform blastoderm, during which cells evenly cover the entirety of the egg. However, the embryo of the German cockroach, Blattella germanica, like those of many insects within the super order Polyneoptera, does not have a uniform blastoderm; instead, its first cells condense rapidly at the site of a future germband. We investigated early development in this species in order to understand how early gene expression is or is not conserved in these insect embryos with distinct early cell behaviors. ResultsWe present a detailed time series of nuclear division and distribution from fertilization through germband formation and report patterns of expression for the early patterning genes hunchback, caudal, and twist in order to understand early polarization and mesoderm formation. We show a detailed time course of the spatial expression of two genes involved in the segmentation cascade, hedgehog and even-skipped, and demonstrate two distinct dynamics of the segmentation process. ConclusionsDespite dramatic differences in cell distribution between the blastoderms of many Polyneopteran insects and those of more well-studied developmental models, expression patterns of early patterning genes are mostly similar. Genes associated with axis determination in other insects are activated relatively late and are probably not maternally deposited. The two phases of segmentation - simultaneous and sequential - might indicate a broadly conserved mode of morphological differentiation. The developmental time course we present here should be of value for further investigation into the causes of this distinct blastoderm type.

developmental biology↗

Development of the Pre-Gnathal Segments of the Insect Head Indicates They Are Not Serial Homologues of Trunk Segments

The three anterior-most segments in arthropods contain the ganglia that make up the arthropod brain. These segments, the pre-gnathal segments, are known to exhibit many developmental differences to other segments, believed to reflect their divergent morphology. We have analyzed the expression and function of the genes involved in the segment-polarity network in the pre-gnathal segments compared with the trunk segments in the hemimetabolous insect Oncopeltus fasciatus. We show that there are fundamental differences in the way the pre-gnathal segments are generated and patterned, relative to all other segments, and that these differences are general to all arthropods. We argue that given these differences, the pre-gnathal segments should not be considered serially homologous to trunk segments. This realization has important implications for our understanding of the evolution of the arthropod head. We suggest a novel scenario for arthropod head evolution that posits duplication of an ancestral single-segmented head into three descendent segments. This scenario is consistent with what we know of head evolution from the fossil record, and helps reconcile some of the debates about early arthropod evolution.

evolutionary biology↗

Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation

One of the best studied developmental processes is the Drosophila segmentation cascade. However, this cascade is generally considered to be highly derived and unusual. We present a detailed analysis of the sequential segmentation cascade of the milkweed bug Oncopletus fasciatus, as a comparison to Drosophila, with the aim of reconstructing the evolution of insect segmentation. We analyzed the expression of 12 genes, representing different phases during segmentation. We reconstruct the spatio-temporal relationships among these genes And their roles and position in the cascade. We conclude that sequential segmentation in the Oncopeltus germband includes three phases: Primary pair-rule genes generate segmental gene expression in the anterior growth zone, followed by secondary pair-rule genes, expressed in the transition between the growth zone and the segmented germband. Segment polarity genes are expressed in the segmented germband. This process generates a single-segment periodicity, and does not have a double-segment pattern at any stage.

developmental biology↗

Elongation during segmentation shows axial variability, low mitotic rates, and synchronized cell cycle domains in the crustacean, Thamnocephalus platyurus

Segmentation in arthropods typically occurs by sequential addition of segments from a posterior growth zone, but cell behaviors producing posterior elongation are not well known. Using precisely staged larvae of the crustacean, Thamnocephalus platyurus, we systematically examined cell division patterns and morphometric changes associated with posterior elongation during segmentation. We show that cell division is required for normal elongation but that cells in the growth zone need only divide ~1.5 times to meet that requirement; correspondingly, direct measures of cell division in the growth zone are low. Morphometric measurements of the growth zone and of newly formed segments suggest tagma-specific features of segment generation. Using methods for detecting two different phases in the cell cycle, we show distinct domains of synchronized cells in the posterior. Borders of cell cycle domains correlate with domains of segmental gene expression, suggesting an intimate link between segment generation and cell cycle regulation.\n\nSummary StatementPosterior growth zone has synchronized cell cycle domains but shows little cell division during segment addition in a crustacean. Dimensions of the shrinking posterior growth zone change at tagma boundaries.

developmental biology↗

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↗