Publications by authors named "Alistair P McGregor"

50 Publications

The evolution of Sox gene repertoires and regulation of segmentation in arachnids.

Mol Biol Evol 2021 Mar 23. Epub 2021 Mar 23.

Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom.

The Sox family of transcription factors regulate many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterising the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterised the Sox repertoires of several arachnid species with and without an ancestral whole genome duplication (WGD), and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We also found that most Sox families have been retained as ohnologs after WGD and evidence for potential subfunctionalization and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete, in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures.
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http://dx.doi.org/10.1093/molbev/msab088DOI Listing
March 2021

A complex gene regulatory architecture underlies the development and evolution of cuticle morphology in Drosophila.

Curr Opin Genet Dev 2021 Jan 30;69:21-27. Epub 2021 Jan 30.

Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE, CONICET-UBA), Buenos Aires 1428, Argentina; Departamento de Ecología, Genética y Evolución (FCEyN, UBA), Buenos Aires 1428, Argentina. Electronic address:

The cuticle of insects is decorated with non-sensory hairs called trichomes. A few Drosophila species independently lost most of the dorso-lateral trichomes on first instar larvae. Genetic experiments revealed that this naked cuticle phenotype was caused by the evolution of enhancer function at the ovo/shavenbaby (ovo/svb) locus. Here we explore how this discovery catalyzed major new insights into morphological evolution in different developmental contexts, enhancer pleiotropy in gene regulation and the functionality and evolution of the Svb gene regulatory network (GRN). Taken together this highlights the importance of understanding the architecture and evolution of gene regulatory networks in detail and the great potential for further study of the Svb GRN.
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http://dx.doi.org/10.1016/j.gde.2021.01.003DOI Listing
January 2021

Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species.

Mol Biol Evol 2021 01;38(2):437-448

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by sexual selection. Mapping studies indicate a highly polygenic and generally additive genetic basis for these morphological differences. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans/D. mauritiana introgression lines on chromosome arm 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the expressed genes and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan (trn), a gene known to contribute to divergence in clasper morphology. Taken together, our results provide new insights into the regulation of genital development and how this has evolved between species.
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http://dx.doi.org/10.1093/molbev/msaa232DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7826188PMC
January 2021

The evolution and development of eye size in flies.

Wiley Interdiscip Rev Dev Biol 2021 Mar 12;10(2):e380. Epub 2020 May 12.

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, UK.

The compound eyes of flies exhibit striking variation in size, which has contributed to the adaptation of these animals to different habitats and their evolution of specialist behaviors. These differences in size are caused by differences in the number and/or size of ommatidia, which are specified during the development of the retinal field in the eye imaginal disc. While the genes and developmental mechanisms that regulate the formation of compound eyes are understood in great detail in the fruit fly Drosophila melanogaster, we know very little about the genetic changes and mechanistic alterations that lead to natural variation in ommatidia number and/or size, and thus overall eye size, within and between fly species. Understanding the genetic and developmental bases for this natural variation in eye size not only has great potential to help us understand adaptations in fly vision but also determine how eye size and organ size more generally are regulated. Here we explore the genetic and developmental mechanisms that could underlie natural differences in compound eye size within and among fly species based on our knowledge of eye development in D. melanogaster and the few cases where the causative genes and mechanisms have already been identified. We suggest that the fly eye provides an evolutionary and developmental framework to better understand the regulation and diversification of this crucial sensory organ globally at a systems level as well as the gene regulatory networks and mechanisms acting at the tissue, cellular and molecular levels. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Invertebrate Organogenesis > Flies Comparative Development and Evolution > Regulation of Organ Diversity.
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http://dx.doi.org/10.1002/wdev.380DOI Listing
March 2021

Wnt gene regulation and function during maxillary palp development in Drosophila melanogaster.

Dev Biol 2020 06 27;462(1):66-73. Epub 2020 Mar 27.

Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom. Electronic address:

Wnt genes encode secreted ligands that play many important roles in the development of metazoans. There are thirteen known Wnt gene subfamilies and seven of these are represented in Drosophila melanogaster. While wingless (wg) is the best understood and most widely studied Wnt gene in Drosophila, the functions of many of the other Drosophila Wnt genes are less well understood. For example, relatively little is known about Wnt6, which is an ancient paralog of wg and they form a conserved Wnt cluster together with Wnt9 (Dwnt4) and Wnt10. Wg and Wnt6 encode similar proteins and exhibit overlapping expression in several tissues during development. Both wg and Wnt6 were previously shown to regulate the development of maxillary palps, important olfactory organs in flies, but it remained unclear how these two ligands may combine to carry out specific functions and how this is regulated. Here, we have further analysed Wnt6 function in the context of maxillary palp development. Surprisingly, we found that Wnt6 does not appear to be necessary for development of maxillary palps. While a deletion of the 5' region of Wnt6 results in very small maxillary palps, we show that this effect is more likely to be a consequence of removing cis-regulatory elements that may regulate wg expression in this tissue rather than through the loss of Wnt6 function. Although, we cannot completely exclude the possibility that Wnt6 may subtly regulate maxillary palp development in combination with wg, our analysis of Wnt6 loss of function mutants suggests this ligand plays a more general role in regulating growth during development. Taken together our results provide new insights into maxillary palp formation and Wnt6 functions in Drosophila, and further evidence for a complex cis-regulatory landscape in the Wnt9-wg-Wnt6-Wnt10 cluster, which may help explain its evolutionary conservation.
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http://dx.doi.org/10.1016/j.ydbio.2020.03.012DOI Listing
June 2020

Gene content evolution in the arthropods.

Genome Biol 2020 01 23;21(1):15. Epub 2020 Jan 23.

Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.

Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.

Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.

Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.
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http://dx.doi.org/10.1186/s13059-019-1925-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6977273PMC
January 2020

Characterization of the Genetic Architecture Underlying Eye Size Variation Within and .

G3 (Bethesda) 2020 03 5;10(3):1005-1018. Epub 2020 Mar 5.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK,

The compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both and This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in and , we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.
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http://dx.doi.org/10.1534/g3.119.400877DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7056968PMC
March 2020

Sensory Organ Size Evolution: A View from Drosophila.

Dev Cell 2019 09;50(6):673-674

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford OX3 0BP, UK. Electronic address:

In this issue of Developmental Cell, Ramaekers et al. (2019) show that changes in eyeless/Pax6 expression cause differences in compound eye size within and between Drosophila species. These findings reveal how changes in the underlying gene regulatory network facilitate eye size evolution and provide insights into organ size regulation.
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http://dx.doi.org/10.1016/j.devcel.2019.09.003DOI Listing
September 2019

underlies the evolution of male genital morphology.

Proc Natl Acad Sci U S A 2019 09 4;116(38):19025-19030. Epub 2019 Sep 4.

Department of Biological and Medical Sciences, Oxford Brookes University, OX3 0BP Oxford, United Kingdom;

Male genital structures are among the most rapidly evolving morphological traits and are often the only features that can distinguish closely related species. This process is thought to be driven by sexual selection and may reinforce species separation. However, while the genetic bases of many phenotypic differences have been identified, we still lack knowledge about the genes underlying evolutionary differences in male genital organs and organ size more generally. The claspers (surstyli) are periphallic structures that play an important role in copulation in insects. Here, we show that divergence in clasper size and bristle number between and is caused by evolutionary changes in (), which encodes a transmembrane leucine-rich repeat domain protein that mediates cell-cell interactions and affinity. There are no fixed amino acid differences in between and , but differences in the expression of this gene in developing genitalia suggest that cis-regulatory changes in underlie the evolution of clasper morphology in these species. Finally, analyses of reciprocal hemizygotes that are genetically identical, except for the species from which the functional allele of originates, determined that the allele of specifies larger claspers with more bristles than the allele of Therefore, we have identified a gene underlying evolutionary change in the size of a male genital organ, which will help to better understand not only the rapid diversification of these structures, but also the regulation and evolution of organ size more broadly.
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http://dx.doi.org/10.1073/pnas.1909829116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6754542PMC
September 2019

A standardized nomenclature and atlas of the male terminalia of .

Fly (Austin) 2019 Mar - Dec;13(1-4):51-64. Epub 2019 Aug 19.

Institut de Systématique, Evolution et Biodiversité, UMR7205, Centre National de la Recherche Scientifique, MNHN, Sorbonne Université, EPHE, Université des Antilles, Paris, France.

Animal terminalia represent some of the most diverse and rapidly evolving structures in the animal kingdom, and for this reason have been a mainstay in the taxonomic description of species. The terminalia of , with its wide range of experimental tools, have recently become the focus of increased interest in the fields of development, evolution, and behavior. However, studies from different disciplines have often used discrepant terminologies for the same anatomical structures. Consequently, the terminology of genital parts has become a barrier to integrating results from different fields, rendering it difficult to determine what parts are being referenced. We formed a consortium of researchers studying the genitalia of to help establish a set of naming conventions. Here, we present a detailed visual anatomy of male genital parts, including a list of synonymous terms, and suggest practices to avoid confusion when referring to anatomical parts in future studies. The goal of this effort is to facilitate interdisciplinary communication and help newcomers orient themselves within the exciting field of genitalia.
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http://dx.doi.org/10.1080/19336934.2019.1653733DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988887PMC
July 2020

Modulation and Evolution of Animal Development through microRNA Regulation of Gene Expression.

Genes (Basel) 2019 04 25;10(4). Epub 2019 Apr 25.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.

microRNAs regulate gene expression by blocking the translation of mRNAs and/or promoting their degradation. They, therefore, play important roles in gene regulatory networks (GRNs) by modulating the expression levels of specific genes and can tune GRN outputs more broadly as part of feedback loops. These roles for microRNAs provide developmental buffering on one hand but can facilitate evolution of development on the other. Here we review how microRNAs can modulate GRNs during animal development as part of feedback loops and through their individual or combinatorial targeting of multiple different genes in the same network. We then explore how changes in the expression of microRNAs and consequently targets can facilitate changes in GRNs that alter development and lead to phenotypic evolution. The reviewed studies exemplify the key roles played by microRNAs in the regulation and evolution of gene expression during developmental processes in animals.
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http://dx.doi.org/10.3390/genes10040321DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6523689PMC
April 2019

Duplication and expression of Sox genes in spiders.

BMC Evol Biol 2018 12 27;18(1):205. Epub 2018 Dec 27.

Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK.

Background: The Sox family of transcription factors is an important part of the genetic 'toolbox' of all metazoans examined to date and is known to play important developmental roles in vertebrates and insects. However, outside the commonly studied Drosophila model little is known about the repertoire of Sox family transcription factors in other arthropod species. Here we characterise the Sox family in two chelicerate species, the spiders Parasteatoda tepidariorum and Stegodyphus mimosarum, which have experienced a whole genome duplication (WGD) in their evolutionary history.

Results: We find that virtually all of the duplicate Sox genes have been retained in these spiders after the WGD. Analysis of the expression of Sox genes in P. tepidariorum embryos suggests that it is likely that some of these genes have neofunctionalised after duplication. Our expression analysis also strengthens the view that an orthologue of vertebrate Group B1 genes, SoxNeuro, is implicated in the earliest events of CNS specification in both vertebrates and invertebrates. In addition, a gene in the Dichaete/Sox21b class is dynamically expressed in the spider segment addition zone, suggestive of an ancient regulatory mechanism controlling arthropod segmentation as recently suggested for flies and beetles. Together with the recent analysis of Sox gene expression in the embryos of other arthropods, our findings support the idea of conserved functions for some of these genes, including a potential role for SoxC and SoxD genes in CNS development and SoxF in limb development.

Conclusions: Our study provides a new chelicerate perspective to understanding the evolution and function of Sox genes and how the retention of duplicates of such important tool-box genes after WGD has contributed to different aspects of spider embryogenesis. Future characterisation of the function of these genes in spiders will help us to better understand the evolution of the regulation of important developmental processes in arthropods and other metazoans including neurogenesis and segmentation.
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http://dx.doi.org/10.1186/s12862-018-1337-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6307133PMC
December 2018

Human eye conditions: insights from the fly eye.

Hum Genet 2019 Sep 1;138(8-9):973-991. Epub 2018 Nov 1.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.

The fruit fly Drosophila melanogaster has served as an excellent model to study and understand the genetics of many human diseases from cancer to neurodegeneration. Studying the regulation of growth, determination and differentiation of the compound eyes of this fly, in particular, have provided key insights into a wide range of diseases. Here we review the regulation of the development of fly eyes in light of shared aspects with human eye development. We also show how understanding conserved regulatory pathways in eye development together with the application of tools for genetic screening and functional analyses makes Drosophila a powerful model to diagnose and characterize the genetics underlying many human eye conditions, such as aniridia and retinitis pigmentosa. This further emphasizes the importance and vast potential of basic research to underpin applied research including identifying and treating the genetic basis of human diseases.
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http://dx.doi.org/10.1007/s00439-018-1948-2DOI Listing
September 2019

A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in a spider.

Elife 2018 08 21;7. Epub 2018 Aug 21.

Laboratory of Evolutionary Developmental Biology, Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

Sox genes encode a set of highly conserved transcription factors that regulate many developmental processes. In insects, the SoxB gene is the only Sox gene known to be involved in segmentation. To determine if similar mechanisms are used in other arthropods, we investigated the role of Sox genes during segmentation in the spider . While does not appear to be involved in spider segmentation, we found that the closely related gene acts as a gap gene during formation of anterior segments and is also part of the segmentation clock for development of the segment addition zone and sequential addition of opisthosomal segments. Thus, we have found that two different mechanisms of segmentation in a non-mandibulate arthropod are regulated by a SoxB gene. Our work provides new insights into the function of an important and conserved gene family, and the evolution of the regulation of segmentation in arthropods.
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http://dx.doi.org/10.7554/eLife.37567DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6167052PMC
August 2018

Homeobox Gene Duplication and Divergence in Arachnids.

Mol Biol Evol 2018 09;35(9):2240-2253

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
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http://dx.doi.org/10.1093/molbev/msy125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107062PMC
September 2018

Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution.

PLoS Genet 2018 05 3;14(5):e1007375. Epub 2018 May 3.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, United Kingdom.

Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary 'hotspots' are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the 'naked valley' on T2 femurs in Drosophila melanogaster is caused by reduced microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.
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http://dx.doi.org/10.1371/journal.pgen.1007375DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5953500PMC
May 2018

The house spider genome reveals an ancient whole-genome duplication during arachnid evolution.

BMC Biol 2017 07 31;15(1):62. Epub 2017 Jul 31.

Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum.

Results: We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication.

Conclusions: Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.
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http://dx.doi.org/10.1186/s12915-017-0399-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5535294PMC
July 2017

Molecular control of gut formation in the spider Parasteatoda tepidariorum.

Genesis 2017 05 22;55(5). Epub 2017 Apr 22.

Laboratório Integrado de Ciências Morfofuncionais, Núcleo em Ecologia e Desenvolvimento Socio-Ambiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro (UFRJ), Macaé, Rio de Janeiro, 27920-560, Brazil.

The development of a digestive system is an essential feature of bilaterians. Studies of the molecular control of gut formation in arthropods have been studied in detail in the fruit fly Drosophila melanogaster. However, little is known in other arthropods, especially in noninsect arthropods. To better understand the evolution of arthropod alimentary system, we investigate the molecular control of gut development in the spider Parasteatoda tepidariorum (Pt), the primary chelicerate model species for developmental studies. Orthologs of the ectodermal genes Pt-wingless (Pt-wg) and Pt-hedgehog (Pt-hh), of the endodermal genes, Pt-serpent (Pt-srp) and Pt-hepatocyte-nuclear factor-4 (Pt-hnf4) and of the mesodermal gene Pt-twist (Pt-twi) are expressed in the same germ layers during spider gut development as in D. melanogaster. Thus, our expression data suggest that the downstream molecular components involved in gut development in arthropods are conserved. However, Pt-forkhead (Pt-fkh) expression and function in spiders is considerably different from its D. melanogaster ortholog. Pt-fkh is expressed before gastrulation in a cell population that gives rise to endodermal and mesodermal precursors, suggesting a possible role for this factor in specification of both germ layers. To test this hypothesis, we knocked down Pt-fkh via RNA interference. Pt-fkh RNAi embryos not only fail to develop a proper gut, but also lack the mesodermal Pt-twi expressing cells. Thus, in spiders Pt-fkh specifies endodermal and mesodermal germ layers. We discuss the implications of these findings for the evolution and development of gut formation in Ecdysozoans.
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http://dx.doi.org/10.1002/dvg.23033DOI Listing
May 2017

Arthropod evolution and development: recent insights from chelicerates and myriapods.

Curr Opin Genet Dev 2016 08 28;39:93-100. Epub 2016 Jun 28.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford OX3 0BP, UK. Electronic address:

Research on arthropod genetics and development has added much to our understanding of animal evolution. While this work has mainly focused on insects, a growing body of research on the less studied myriapods and chelicerates is providing important new insights into arthropod genomics and development. Multiple chelicerate lineages have a high incidence of gene duplication, which is suggestive of large-scale and even whole genome duplications. Furthermore, the duplication and divergence of genes is associated with the evolution of appendage morphology and other phenotypes in chelicerates and myriapods. Recent studies of these arthropods have also helped to understand the evolution and development of segmented bodies. Further research on chelicerate and myriapod models as well as species from other orders of these subphyla has great potential to expand our understanding of the evolution of animal genomes and development.
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http://dx.doi.org/10.1016/j.gde.2016.06.002DOI Listing
August 2016

Pervasive microRNA Duplication in Chelicerates: Insights from the Embryonic microRNA Repertoire of the Spider Parasteatoda tepidariorum.

Genome Biol Evol 2016 08 3;8(7):2133-44. Epub 2016 Aug 3.

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, United Kingdom

MicroRNAs are small (∼22 nt) noncoding RNAs that repress translation and therefore regulate the production of proteins from specific target mRNAs. microRNAs have been found to function in diverse aspects of gene regulation within animal development and many other processes. Among invertebrates, both conserved and novel, lineage specific, microRNAs have been extensively studied predominantly in holometabolous insects such as Drosophila melanogaster However little is known about microRNA repertoires in other arthropod lineages such as the chelicerates. To understand the evolution of microRNAs in this poorly sampled subphylum, we characterized the microRNA repertoire expressed during embryogenesis of the common house spider Parasteatoda tepidariorum We identified a total of 148 microRNAs in P. tepidariorum representing 66 families. Approximately half of these microRNA families are conserved in other metazoans, while the remainder are specific to this spider. Of the 35 conserved microRNAs families 15 had at least two copies in the P. tepidariorum genome. A BLAST-based approach revealed a similar pattern of duplication in other spiders and a scorpion, but not among other chelicerates and arthropods, with the exception of a horseshoe crab. Among the duplicated microRNAs we found examples of lineage-specific tandem duplications, and the duplication of entire microRNA clusters in three spiders, a scorpion, and in a horseshoe crab. Furthermore, we found that paralogs of many P. tepidariorum microRNA families exhibit arm switching, which suggests that duplication was often followed by sub- or neofunctionalization. Our work shows that understanding the evolution of microRNAs in the chelicerates has great potential to provide insights into the process of microRNA duplication and divergence and the evolution of animal development.
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http://dx.doi.org/10.1093/gbe/evw143DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4987109PMC
August 2016

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum.

Development 2016 07 10;143(13):2455-63. Epub 2016 Jun 10.

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford OX3 0BP, UK

In short-germ arthropods, posterior segments are added sequentially from a segment addition zone (SAZ) during embryogenesis. Studies in spiders such as Parasteatoda tepidariorum have provided insights into the gene regulatory network (GRN) underlying segment addition, and revealed that Wnt8 is required for dynamic Delta (Dl) expression associated with the formation of new segments. However, it remains unclear how these pathways interact during SAZ formation and segment addition. Here, we show that Delta-Notch signalling is required for Wnt8 expression in posterior SAZ cells, but represses the expression of this Wnt gene in anterior SAZ cells. We also found that these two signalling pathways are required for the expression of the spider orthologues of even-skipped (eve) and runt-1 (run-1), at least in part via caudal (cad). Moreover, it appears that dynamic expression of eve in this spider does not require a feedback loop with run-1, as is found in the pair-rule circuit of the beetle Tribolium Taken together, our results suggest that the development of posterior segments in Parasteatoda is directed by dynamic interactions between Wnt8 and Delta-Notch signalling that are read out by cad, which is necessary but probably not sufficient to regulate the expression of eve and run-1 Our study therefore provides new insights towards better understanding the evolution and developmental regulation of segmentation in other arthropods, including insects.
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http://dx.doi.org/10.1242/dev.131656DOI Listing
July 2016

A robust (re-)annotation approach to generate unbiased mapping references for RNA-seq-based analyses of differential expression across closely related species.

BMC Genomics 2016 05 24;17:392. Epub 2016 May 24.

Georg-August-Universität Göttingen, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Göttingen, Germany.

Background: RNA-seq based on short reads generated by next generation sequencing technologies has become the main approach to study differential gene expression. Until now, the main applications of this technique have been to study the variation of gene expression in a whole organism, tissue or cell type under different conditions or at different developmental stages. However, RNA-seq also has a great potential to be used in evolutionary studies to investigate gene expression divergence in closely related species.

Results: We show that the published genomes and annotations of the three closely related Drosophila species D. melanogaster, D. simulans and D. mauritiana have limitations for inter-specific gene expression studies. This is due to missing gene models in at least one of the genome annotations, unclear orthology assignments and significant gene length differences in the different species. A comprehensive evaluation of four statistical frameworks (DESeq2, DESeq2 with length correction, RPKM-limma and RPKM-voom-limma) shows that none of these methods sufficiently accounts for inter-specific gene length differences, which inevitably results in false positive candidate genes. We propose that published reference genomes should be re-annotated before using them as references for RNA-seq experiments to include as many genes as possible and to account for a potential length bias. We present a straight-forward reciprocal re-annotation pipeline that allows to reliably compare the expression for nearly all genes annotated in D. melanogaster.

Conclusions: We conclude that our reciprocal re-annotation of previously published genomes facilitates the analysis of significantly more genes in an inter-specific differential gene expression study. We propose that the established pipeline can easily be applied to re-annotate other genomes of closely related animals and plants to improve comparative expression analyses.
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http://dx.doi.org/10.1186/s12864-016-2646-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4877740PMC
May 2016

Genetic architecture and functional characterization of genes underlying the rapid diversification of male external genitalia between Drosophila simulans and Drosophila mauritiana.

Genetics 2015 May 16;200(1):357-69. Epub 2015 Mar 16.

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom

Male sexual characters are often among the first traits to diverge between closely related species and identifying the genetic basis of such changes can contribute to our understanding of their evolutionary history. However, little is known about the genetic architecture or the specific genes underlying the evolution of male genitalia. The morphology of the claspers, posterior lobes, and anal plates exhibit striking differences between Drosophila mauritiana and D. simulans. Using QTL and introgression-based high-resolution mapping, we identified several small regions on chromosome arms 3L and 3R that contribute to differences in these traits. However, we found that the loci underlying the evolution of clasper differences between these two species are independent from those that contribute to posterior lobe and anal plate divergence. Furthermore, while most of the loci affect each trait in the same direction and act additively, we also found evidence for epistasis between loci for clasper bristle number. In addition, we conducted an RNAi screen in D. melanogaster to investigate if positional and expression candidate genes located on chromosome 3L, are also involved in genital development. We found that six of these genes, including components of Wnt signaling and male-specific lethal 3 (msl3), regulate the development of genital traits consistent with the effects of the introgressed regions where they are located and that thus represent promising candidate genes for the evolution these traits.
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http://dx.doi.org/10.1534/genetics.114.174045DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4423377PMC
May 2015

From shavenbaby to the naked valley: trichome formation as a model for evolutionary developmental biology.

Evol Dev 2015 Jan-Feb;17(1):120-6

Friedrich Meischer Laboratory of the Max Planck Society, Spemannstrasse 39, Tuebingen, 72076, Germany.

Microtrichia or trichomes are non-sensory actin protrusions produced by the epidermal cells of many insects. Studies of trichome formation in Drosophila have over the last 30 years provided key insights towards our understanding of gene regulation, gene regulatory networks (GRNs), development, the genotype to phenotype map, and the evolution of these processes. Here we review classic studies that have used trichome formation as a model to shed light on Drosophila development as well as recent research on the architecture of the GRN underlying trichome formation. This includes the findings that both small peptides and microRNAs play important roles in the regulation and evolution of this network. In addition, we review research on the evolution of trichome patterns that has provided novel insights into the function and architecture of cis-regulatory modules, and into the genetic basis of morphological change. We conclude that further research on these apparently simple and often functionally enigmatic structures will continue to provide new and important knowledge about development and evolution.
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http://dx.doi.org/10.1111/ede.12113DOI Listing
May 2015

Low affinity binding site clusters confer hox specificity and regulatory robustness.

Cell 2015 Jan 31;160(1-2):191-203. Epub 2014 Dec 31.

Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, USA. Electronic address:

In animals, Hox transcription factors define regional identity in distinct anatomical domains. How Hox genes encode this specificity is a paradox, because different Hox proteins bind with high affinity in vitro to similar DNA sequences. Here, we demonstrate that the Hox protein Ultrabithorax (Ubx) in complex with its cofactor Extradenticle (Exd) bound specifically to clusters of very low affinity sites in enhancers of the shavenbaby gene of Drosophila. These low affinity sites conferred specificity for Ubx binding in vivo, but multiple clustered sites were required for robust expression when embryos developed in variable environments. Although most individual Ubx binding sites are not evolutionarily conserved, the overall enhancer architecture-clusters of low affinity binding sites-is maintained and required for enhancer function. Natural selection therefore works at the level of the enhancer, requiring a particular density of low affinity Ubx sites to confer both specific and robust expression.
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http://dx.doi.org/10.1016/j.cell.2014.11.041DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4449256PMC
January 2015

Sexual dimorphism and natural variation within and among species in the Drosophila retinal mosaic.

BMC Evol Biol 2014 Nov 26;14:240. Epub 2014 Nov 26.

Background: Insect compound eyes are composed of ommatidia, which contain photoreceptor cells that are sensitive to different wavelengths of light defined by the specific rhodopsin proteins that they express. The fruit fly Drosophila melanogaster has several different ommatidium types that can be localised to specific retinal regions, such as the dorsal rim area (DRA), or distributed stochastically in a mosaic across the retina, like the 'pale' and 'yellow' types. Variation in these ommatidia patterns very likely has important implications for the vision of insects and could underlie behavioural and environmental adaptations. However, despite the detailed understanding of ommatidia specification in D. melanogaster, the extent to which the frequency and distribution of the different ommatidium types vary between sexes, strains and species of Drosophila is not known.

Results: We investigated the frequency and distribution of ommatidium types based on rhodopsin protein expression, and the expression levels of rhodopsin transcripts in the eyes of both sexes of different strains of D. melanogaster, D. simulans and D. mauritiana. We found that while the number of DRA ommatidia was invariant, Rh3 expressing ommatidia were more frequent in the larger eyes of females compared to the males of all species analysed. The frequency and distribution of ommatidium types also differed between strains and species. The D. simulans strain ZOM4 has the highest frequency of Rh3 expressing ommatidia, which is associated with a non-stochastic patch of pale and odd-coupled ommatidia in the dorsal-posterior of their eyes.

Conclusions: Our results show that there is striking variation in the frequency and distribution of ommatidium types between sexes, strains and species of Drosophila. This suggests that evolutionary changes in the underlying regulatory mechanisms can alter the distribution of ommatidium types to promote or restrict their expression in specific regions of the eye within and between species, and that this could cause differences in vision among these flies.
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http://dx.doi.org/10.1186/s12862-014-0240-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4268811PMC
November 2014

A comprehensive reference transcriptome resource for the common house spider Parasteatoda tepidariorum.

PLoS One 2014 13;9(8):e104885. Epub 2014 Aug 13.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America.

Parasteatoda tepidariorum is an increasingly popular model for the study of spider development and the evolution of development more broadly. However, fully understanding the regulation and evolution of P. tepidariorum development in comparison to other animals requires a genomic perspective. Although research on P. tepidariorum has provided major new insights, gene analysis to date has been limited to candidate gene approaches. Furthermore, the few available EST collections are based on embryonic transcripts, which have not been systematically annotated and are unlikely to contain transcripts specific to post-embryonic stages of development. We therefore generated cDNA from pooled embryos representing all described embryonic stages, as well as post-embryonic stages including nymphs, larvae and adults, and using Illumina HiSeq technology obtained a total of 625,076,514 100-bp paired end reads. We combined these data with 24,360 ESTs available in GenBank, and 1,040,006 reads newly generated from 454 pyrosequencing of a mixed-stage embryo cDNA library. The combined sequence data were assembled using a custom de novo assembly strategy designed to optimize assembly product length, number of predicted transcripts, and proportion of raw reads incorporated into the assembly. The de novo assembly generated 446,427 contigs with an N50 of 1,875 bp. These sequences obtained 62,799 unique BLAST hits against the NCBI non-redundant protein data base, including putative orthologs to 8,917 Drosophila melanogaster genes based on best reciprocal BLAST hit identity compared with the D. melanogaster proteome. Finally, we explored the utility of the transcriptome for RNA-Seq studies, and showed that this resource can be used as a mapping scaffold to detect differential gene expression in different cDNA libraries. This resource will therefore provide a platform for future genomic, gene expression and functional approaches using P. tepidariorum.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0104885PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4132015PMC
May 2015

Analysis of the Wnt gene repertoire in an onychophoran provides new insights into the evolution of segmentation.

Evodevo 2014 Apr 3;5(1):14. Epub 2014 Apr 3.

Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, Uppsala, 75236, Sweden.

Background: The Onychophora are a probable sister group to Arthropoda, one of the most intensively studied animal phyla from a developmental perspective. Pioneering work on the fruit fly Drosophila melanogaster and subsequent investigation of other arthropods has revealed important roles for Wnt genes during many developmental processes in these animals.

Results: We screened the embryonic transcriptome of the onychophoran Euperipatoides kanangrensis and found that at least 11 Wnt genes are expressed during embryogenesis. These genes represent 11 of the 13 known subfamilies of Wnt genes.

Conclusions: Many onychophoran Wnt genes are expressed in segment polarity gene-like patterns, suggesting a general role for these ligands during segment regionalization, as has been described in arthropods. During early stages of development, Wnt2, Wnt4, and Wnt5 are expressed in broad multiple segment-wide domains that are reminiscent of arthropod gap and Hox gene expression patterns, which suggests an early instructive role for Wnt genes during E. kanangrensis segmentation.
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http://dx.doi.org/10.1186/2041-9139-5-14DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4021614PMC
April 2014

A perspective on micro-evo-devo: progress and potential.

Genetics 2013 Nov;195(3):625-34

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford OX3 0BP, United Kingdom.

The term "micro-evo-devo" refers to the combined study of the genetic and developmental bases of natural variation in populations and the evolutionary forces that have shaped this variation. It thus represents a synthesis of the fields of evolutionary developmental biology and population genetics. As has been pointed out by several others, this synthesis can provide insights into the evolution of organismal form and function that have not been possible within these individual disciplines separately. Despite a number of important successes in micro-evo-devo, however, it appears that evo devo and population genetics remain largely separate spheres of research, limiting their ability to address evolutionary questions. This also risks pushing contemporary evo devo to the fringes of evolutionary biology because it does not describe the causative molecular changes underlying evolution or the evolutionary forces involved. Here we reemphasize the theoretical and practical importance of micro-evo-devo as a strategy for understanding phenotypic evolution, review the key recent insights that it has provided, and present a perspective on both the potential and the remaining challenges of this exciting interdisciplinary field.
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http://dx.doi.org/10.1534/genetics.113.156463DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3813853PMC
November 2013

Genetic and developmental analysis of differences in eye and face morphology between Drosophila simulans and Drosophila mauritiana.

Evol Dev 2013 Jul-Aug;15(4):257-67. Epub 2013 May 16.

Max Planck Institute for Biology of Ageing, Robert‐Koch‐Straße 21, D‐50931 Cologne, Germany.

Eye and head morphology vary considerably among insects and even between closely related species of Drosophila. Species of the D. melanogaster subgroup, and other Drosophila species, exhibit a negative correlation between eye size and face width (FW); for example, D. mauritiana generally has bigger eyes composed of larger ommatidia and conversely a narrower face than its sibling species. To better understand the evolution of eye and head morphology, we investigated the genetic and developmental basis of differences in eye size and FW between male D. mauritiana and D. simulans. QTL mapping of eye size and FW showed that the major loci responsible for the interspecific variation in these traits are localized to different genomic regions. Introgression of the largest effect QTL underlying the difference in eye size resulted in flies with larger eyes but no significant difference in FW. Moreover,introgression of a QTL region on the third chromosome that contributes to the FW difference between these species affected FW, but not eye size. We also observed that this difference in FW is detectable earlier in the development of the eye‐antennal disc than the difference in the size of the retinal field. Our results suggest that different loci that act at different developmental stages underlie changes in eye size and FW. Therefore, while there is a negative correlation between these traits in Drosophila, we show genetically that they also have the potential to evolve independently and this may help to explain the evolution of these traits in other insects.
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http://dx.doi.org/10.1111/ede.12027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3799016PMC
October 2013