Biology subjects

Holland, P. W. H.

Publications and source records attributed to Holland, P. W. H..

8 recordsLinked to original sources

bioRxiv2026

Cryptic whole-genome duplication in bryozoans

Whole-genome duplications (WGDs) have long been proposed as evolutionary facilitators of biological complexity and diversification. Ancient WGDs occurred deep in the evolutionary history of both plants and vertebrates, but appear to be rare in invertebrates. However, it is unclear whether this reflects genuine scarcity or inadequate detection methodologies, and current methods may be insufficient to detect very old WGDs where extensive gene loss has followed. Here, we used a combination of paralogous and orthologous synteny-based methods incorporating bilaterian ancestral linkage groups (ALGs) to search for genomic signatures of WGD in members of the invertebrate phylum Bryozoa. This revealed strong evidence for an ancient WGD in the freshwater bryozoan Cristatella mucedo, Class Phylactolaemata, with duplicated paralogous regions across every chromosome. Only ~10% of duplicated genes are retained, including a Hox cluster duplication. All eight genomes from the bryozoan class Gymnolaemata also show signatures of ancient WGD in the form of 2:1 ratios in orthologous synteny comparisons, which remain detectable despite only ~5% duplicate retention. Gene trees support a scenario in which all extant bryozoans share an ancient WGD and much of the genome rediploidised independently in the two clades. Duplicates retained after bryozoan WGD are enriched in cilia genes and are preferentially expressed in the lophophore, the tentacular feeding organ covered in highly specialised cilia. We argue that cryptic WGD in bryozoan evolution facilitated adaptation to a sessile, filter-feeding lifestyle, and propose that incorporation of ALGs adds to the power of synteny-based WGD-detection methods.

genomics↗

bioRxiv2025

Revised evolutionary relationships within Brachycera and the early origin of bicoid in flies

The specification of the anterior-posterior axis in the embryo is a crucial step in early insect development. Despite its importance, the underlying genetic and regulatory architecture controlling this process varies significantly between species. In cyclorrhaphan flies, such as Drosophila melanogaster, anterior determination is controlled by the transcription factor bicoid, which emerged through duplication of the ancestral Hox3 gene (called zen in insects). With new, high-quality genomic data we mine the genomes of 186 dipteran species, and find presence of bicoid in non-cyclorrhaphan flies, including in the bee flies (family Bombyliidae) and the stiletto flies (Therevidae). We confirm maternal expression and localisation of the non-cyclorrhaphan bicoid mRNA to the anterior region of the unfertilised oocyte in the dark edged bee fly, Bombylius major. To determine the timing and origin of bicoid, we address uncertainty in the dipteran phylogeny, uncovering a ladder-like topology in the branching orders of the early Brachycera lineages. This new species phylogeny suggests that bicoid emerged at the common ancestor of Bombyliidae, Asiloidea, and Eremoneura (collectively Heterodactyla), and was subsequently lost at least 16 times. These findings expand our understanding of the early developmental processes in flies and provide new insights into the backbone phylogeny of Diptera and the evolution of bicoid.

evolutionary biology↗

bioRxiv2024

Brachiopod genome unveils the evolution of the BMP-Chordin network in bilaterian body patterning

Bone morphogenetic protein (BMP) signalling is crucial in regulating dorsal-ventral patterning and cell fate determination during early development in bilaterians. Interactions between BMP ligands and their main antagonist, Chordin, establish BMP gradients, subdivide embryos into distinct territories and organise body plans. However, the molecular control and evolutionary origins of dorsal-ventral patterning within spiralians, one of the three major bilaterian groups, have been obscured by their unique embryonic development. Here we present the chromosome-level genome of a spiralian with deuterostome-like development, the brachiopod Lingula anatina, and apply functional transcriptomics to study dorsal-ventral patterning under the control of BMP signalling. We uncover the presence of a dorsal-ventral BMP signalling gradient in the L. anatina gastrula with bmp2/4 and chordin expressed at its dorsal and ventral sides, respectively. Using small-molecule drugs, exogenous recombinant BMP proteins and RNA sequencing, we show that a high level of BMP pathway activation inhibits the expression of neural genes during gastrula and larval stages. We also show that BMP signalling splits the developing larval shell field into two valves. The discovery of a BMP-mediated dorsal-ventral patterning system in a spiralian, similar to those observed in deuterostomes and non-spiralian protostomes, suggests deep conservation of this mechanism across all three major bilaterian clades. This is further supported by striking similarities in the gene sets regulated by BMP signalling in brachiopods and the vertebrate model Xenopus. We argue that the spiralian ancestor retained the basal bilaterian mechanism of dorsal-ventral patterning, although downstream components of the BMP-Chordin network have undergone dynamic evolutionary changes.

evolutionary biology↗

bioRxiv2024

Fusion, fission, and scrambling of the bilaterian genome in Bryozoa

Groups of orthologous genes are commonly found together on the same chromosome over vast evolutionary distances. This extensive physical gene linkage, known as macrosynteny, is seen between bilaterian phyla as divergent as Chordata, Echinodermata, Mollusca, and Nemertea. Here, we report a unique pattern of genome evolution in Bryozoa, an understudied phylum of colonial invertebrates. Using comparative genomics, we reconstruct the chromosomal evolutionary history of five bryozoans. Multiple ancient chromosome fusions followed by gene mixing led to the near-complete loss of bilaterian linkage groups in the ancestor of extant bryozoans. A second wave of rearrangements, including chromosome fission, then occurred independently in two bryozoan classes, further scrambling bryozoan genomes. We also discover at least five derived chromosomal fusion events shared between bryozoans and brachiopods, supporting the traditional but highly debated Lophophorata hypothesis. Finally, we show that chromosome fusion and fission processes led to the partitioning of genes from bryozoan Hox clusters onto multiple chromosomes. Our findings demonstrate that the canonical bilaterian genome structure has been lost across all studied representatives of an entire phylum; reveal that linkage group fission can occur very frequently in specific lineages; and provide a powerful source of phylogenetic information.

evolutionary biology↗

bioRxiv2023

GC content across insect genomes: phylogenetic patterns, causes and consequences

The proportions of A:T and G:C nucleotide pairs are often unequal and can vary greatly between animal species and along chromosomes. The causes and consequences of this variation are incompletely understood. The recent release of high-quality genome sequences from the Darwin Tree of Life and other large-scale genome projects provides an opportunity for GC heterogeneity to be compared across a large number of insect species. Here we analyse GC content along chromosomes, and within protein-coding genes and codons, of 150 insect species from four holometabolous orders: Coleoptera, Diptera, Hymenoptera, and Lepidoptera. We find that protein-coding sequences have higher GC content than the genome average, and that Lepidoptera generally have higher GC content than the other three insect orders examined. GC content is higher in small chromosomes in most Lepidoptera species, but this pattern is less consistent in other orders. GC content also increases towards subtelomeric regions within protein-coding genes in Hymenoptera, Coleoptera and, most strikingly, Lepidoptera. Two species of Diptera, Bombylius major and B. discolor, have very atypical genomes with ubiquitous increase in AT content, especially at third codon positions. Despite dramatic AT-biased codon usage, we find no evidence that this has driven divergent protein evolution. We argue that the GC landscape of Lepidoptera, Hymenoptera and Coleoptera genomes is influenced by GC-biased gene conversion, strongest in Lepidoptera, with some outlier taxa affected drastically by counteracting processes.

evolutionary biology↗

bioRxiv2023

Opsin gene duplication in Lepidoptera: retrotransposition, sex linkage, and gene expression

Colour vision in insects is determined by signalling cascades, central to which are opsin proteins, resulting in sensitivity to light at different wavelengths. In certain insect groups, lineage specific evolution of opsin genes, in terms of copy number, shifts in expression patterns, and functional amino acid substitutions, has resulted in changes in colour vision with subsequent behavioural and niche adaptations. Lepidoptera are a fascinating model to address whether evolutionary change in opsin content and sequence evolution are associated with changes in vision phenotype. Until recently, the lack of high quality genome data representing broad sampling across the lepidopteran phylogeny has greatly limited our ability to accurately address this question. Here, we annotate opsin genes in 219 lepidopteran genomes representing 33 families, reconstruct their evolutionary history, and analyse shifts in selective pressures and expression between genes and species. We discover 44 duplication events in opsin genes across [~]300 million years of lepidopteran evolution. While many duplication events are species or family specific, we find retention of an ancient long-wavelength sensitive (LW) opsin duplication derived by retrotransposition within the speciose superfamily Noctuoidea (in the families Nolidae, Erebidae, and Noctuidae). This conserved LW retrogene shows life stage specific expression suggesting visual sensitivities or other sensory functions specific to the early larval stage. This study provides a comprehensive order-wide view of opsin evolution across Lepidoptera, showcasing high rates of opsin duplications and changes in expression patterns.

evolutionary biology↗

bioRxiv2023

Rapid evolution of the embryonically-expressed homeobox gene LEUTX within primates

LEUTX is a homeodomain transcription factor expressed in the very early embryo with a function around embryonic genome activation. The LEUTX gene is found only in eutherian mammals, including humans, but unlike the majority of homeobox genes, the encoded amino acid sequence is very different between divergent mammalian species. However, whether dynamic evolution has also occurred between closely related mammalian species remains unclear. In this work, we perform a comparative genomics study of LEUTX within the primates, revealing dramatic evolutionary sequence change between closely related species. Positive selection has acted on sites in the LEUTX protein, including six sites within the homeodomain; this suggests that selection may have driven changes in the set of downstream targets. Transfection into cell culture followed by transcriptomic analysis reveals small functional differences between human and marmoset LEUTX, suggesting rapid sequence evolution has fine-tuned the role of this homeodomain protein within the primates. SignificanceHomeobox genes are key regulators of animal development and are therefore often highly conserved between divergent species. However, recent work has uncovered several apparently fast-evolving homeobox genes expressed during mammalian development, one of which is LEUTX. Here we show that the LEUTX genes of primates are highly variable, and that these sequence changes have resulted in small modifications to its protein function. This continued rapid divergence of an embryonic gene between closely related species is significant to the areas of evolutionary, developmental and genome biology.

evolutionary biology↗

bioRxiv2016

Genome sequence of a diabetes-prone desert rodent reveals a mutation hotspot around the ParaHox gene cluster

The sand rat Psammomys obesus is a gerbil native to deserts of North Africa and the Middle East1. Sand rats survive with low caloric intake and when given high carbohydrate diets can become obese and develop type II diabetes2 which, in extreme cases, leads to pancreatic failure and death3,4. Previous studies have reported inability to detect the Pdx1 gene or protein in gerbils5-7, suggesting that absence of this key insulin-regulating homeobox gene might underlie diabetes susceptibility. Here we report sequencing of the sand rat genome and discovery of an extensive, mutationally-biased GC-rich genomic domain encompassing many essential genes, including the elusive Pdx1. The sequence of Pdx1 has been grossly affected by GC-biased mutation leading to the highest divergence observed in the animal kingdom. In addition to molecular insights into restricted caloric intake in a desert species, the discovery that specific chromosomal regions can be subject to elevated mutation rate has widespread significance to evolution.

evolutionary biology↗