Homology of process: developmental dynamics in comparative biology

Comparative biology builds up systematic knowledge of the diversity of life, across evolutionary lineages and levels of organization, starting with evidence from a sparse sample of model organisms. In developmental biology, a key obstacle to the growth of comparative approaches is that the concept of homology is not very well defined for levels of organization that are intermediate between individual genes and morphological characters. In this paper, we investigate what it means for ontogenetic processes to be homologous, focusing specifically on the examples of insect segmentation and vertebrate somitogenesis. These processes can be homologous without homology of the underlying genes or gene networks, since the latter can diverge over evolutionary time, while the dynamics of the process remain the same. Ontogenetic processes like these therefore constitute a dissociable level and distinctive unit of comparison requiring their own specific criteria of homology. In addition, such processes are typically complex and nonlinear, such that their rigorous description and comparison requires not only observation and experimentation, but also dynamical modelling. We propose six criteria of process homology, combining recognized indicators (sameness of parts, morphological outcome and topological position) with novel ones derived from dynamical systems modelling (sameness of dynamical properties, dynamical complexity and evidence for transitional forms). We show how these criteria apply to animal segmentation and other ontogenetic processes. We conclude by situating our proposed dynamical framework for homology of process in relation to similar research programmes, such as process structuralism and developmental approaches to morphological homology.

Download Full-text

Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2007.2245 ◽

2008 ◽

Vol 363 (1496) ◽

pp. 1549-1556 ◽

Cited By ~ 28

Author(s):

Suzanne V Saenko ◽

Vernon French ◽

Paul M Brakefield ◽

Patrícia Beldade

Keyword(s):

Gene Networks ◽

Evolutionary Developmental Biology ◽

Model Organisms ◽

Bicyclus Anynana ◽

Developmental Processes ◽

Key Issues ◽

Or Gene ◽

Morphological Novelties ◽

Shed Light ◽

Evolutionary Novelties

The origin and diversification of evolutionary novelties—lineage-specific traits of new adaptive value—is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development.

Download Full-text

Nonhuman primates’ tissue banks: resources for all model organism research

Mammalian Genome ◽

10.1007/s00335-021-09925-w ◽

2021 ◽

Author(s):

Claire Witham ◽

Sara Wells

Keyword(s):

Nonhuman Primates ◽

Ex Vivo ◽

Model Organism ◽

Translation Studies ◽

Model Organisms ◽

Laboratory Animals ◽

Tissue Banks ◽

Post Mortem ◽

Wide Range ◽

Research Programmes

AbstractBiobanks containing tissue and other biological samples from many model organisms provide easy and faster access to ex vivo resources for a wide-range of research programmes. For all laboratory animals, collecting and preserving tissue at post-mortem is an effective way of maximising the benefits of individual animals and potentially reducing the numbers required for experimentation in the future. For primate tissues, biobanks represent the scarcest of these resources but quite possibly those most valuable for preclinical and translation studies.

Download Full-text

Terrestrial Environments

Evolution and Biogeography ◽

10.1093/oso/9780190637842.003.0014 ◽

2020 ◽

pp. 359-388

Author(s):

Spyros Sfenthourakis ◽

Alan A. Myers ◽

Stefano Taiti ◽

James K. Lowry

Keyword(s):

Morphological Characters ◽

Tectonic Activity ◽

Model Organisms ◽

Aquatic Life ◽

Terrestrial Isopods ◽

Biological Studies ◽

The Family ◽

Terrestrial Environments ◽

Forest Leaf Litter ◽

Almost All

Among crustaceans, only Amphipoda, Isopoda, and Decapoda have invaded truly terrestrial environments, but only two groups show full adaptations to live on land: the family Talitridae among the Amphipoda and the suborder Oniscidea among the Isopoda. The Talitridae occur primarily in forest leaf litter, but a number of other habitats, including caves, are recorded. Talitrids are important ecological contributors to the litter fauna, often occurring in high densities. Their adaptations to a terrestrial way of life include the retention of the mitten-shaped second gnathopods, a neotenic condition among males; the first article of antenna 2 greatly enlarged and fixed to the side of the head; and enlarged gills and pleopods often reduced, sometimes to vestigial stumps. Talitrids have a skewed world distribution being at their most diverse in New Zealand, Tasmania, and Japan/Taiwan. They occur in the Caribbean and Central America but are absent from South and North America except as introduced taxa. Their distribution is largely a result of tectonic activity during the past 150 million years and of extinctions during the Tertiary due to increasing aridity of the climate. The Oniscidea (terrestrial isopods) are the only crustaceans that have managed to adapt to almost all habitat types on land and have become the most species-rich suborder of Isopoda. Although monophyly of the Oniscidea is generally accepted, current taxonomy, based almost entirely on morphological characters, needs extensive revision. Terrestrial isopods present a number of unique adaptations to life on land, some of which result from what can be considered as pre-adaptations of ancestral marine isopods, such as egg development in a marsupium, being dorso-ventrally oblate and having a pleopodal respiration. Other crucial adaptations of Oniscidea include the water-conducting system, the structure of their cuticle, and the “covered” type of pleopodal lungs, all of which are responses to the acute problem of desiccation. They are also among the most speciose taxa in caves, some species have even returned to an aquatic life, and a few species have evolved social behavior. Oniscidea are increasingly being used in biogeographical, phylogeographical, ecological, and evolutionary research and can become model organisms for a broad range of biological studies.

Download Full-text

Transcriptome Analysis in Domesticated Species: Challenges and Strategies

Bioinformatics and Biology Insights ◽

10.4137/bbi.s29334 ◽

2015 ◽

Vol 9S4 ◽

pp. BBI.S29334 ◽

Cited By ~ 4

Author(s):

Jessica P. Hekman ◽

Jennifer L Johnson ◽

Anna V. Kukekova

Keyword(s):

Complex Traits ◽

Gene Networks ◽

Association Studies ◽

Cultural Value ◽

Genomic Research ◽

Model Organisms ◽

Genome Wide Association Studies ◽

Rna Seq ◽

Genome Wide ◽

Genome Assemblies

Domesticated species occupy a special place in the human world due to their economic and cultural value. In the era of genomic research, domesticated species provide unique advantages for investigation of diseases and complex phenotypes. RNA sequencing, or RNA-seq, has recently emerged as a new approach for studying transcriptional activity of the whole genome, changing the focus from individual genes to gene networks. RNA-seq analysis in domesticated species may complement genome-wide association studies of complex traits with economic importance or direct relevance to biomedical research. However, RNA-seq studies are more challenging in domesticated species than in model organisms. These challenges are at least in part associated with the lack of quality genome assemblies for some domesticated species and the absence of genome assemblies for others. In this review, we discuss strategies for analyzing RNA-seq data, focusing particularly on questions and examples relevant to domesticated species.

Download Full-text

Spines and homologues in ‘araphid’ diatoms

Plant Ecology and Evolution ◽

10.5091/plecevo.2019.1597 ◽

2019 ◽

Vol 152 (2) ◽

pp. 150-162 ◽

Cited By ~ 4

Author(s):

David M. Williams

Keyword(s):

Morphological Characters ◽

Comparative Biology ◽

Molecular Trees ◽

As If

Background and aims – Many diatoms have spines on the surface of their valves. These structures differ from one taxon to another. Are all these spines the same? Are they homologues of one another? This paper sets out to explore some of the issues surrounding the determination of homologues with reference to members of Fragilariaceae. Methods – A variety of spines from species in Fragilariaceae are examined (in the SEM) and position on the valve documented relative to those already recorded in the literature. Key results – Spines that occur on the valves of some ‘araphid’ diatoms in Fragilariaceae can be interpreted in the light of where they are found. Spines that occur on the virgae can be thought of as modifications of that structure; spines that occur on the vimines can be thought of as modifications of that structure – the two kinds of spines are not homologues of each other. The term ‘spine’, on its own, is not useful for understanding taxon relationships; the term ‘spine’ is not even a character in the comparative biology sense but a descriptive catch-all for something that simply ‘sticks out from a surface’. Conclusions – Systematic characters, those applicable to comparative biology, are modifications of other characters and so are, in one sense, like taxonomies: hierarchical. A consequence of this is that plotting morphological characters on molecular trees of relationships is a futile endeavour – treating characters and their modifications, as if they are static (unit) features of a non-changing entity, is book-keeping not science.

Download Full-text

Diverse biological processes coordinate the transcriptional response to nutritional changes in a Drosophila melanogaster multiparent population

10.1101/712984 ◽

2019 ◽

Author(s):

E. Ng’oma ◽

P.A. Williams-Simon ◽

A. Rahman ◽

E.G. King

Keyword(s):

Gene Expression ◽

Gene Networks ◽

Sequence Data ◽

Nutrient Sensing ◽

Gene Set Enrichment Analysis ◽

Tissue Type ◽

Model Organisms ◽

Laboratory Model ◽

Fisher Exact Test ◽

Tissue Samples

AbstractBackgroundEnvironmental variation in the amount of resources available to populations challenge individuals to optimize the allocation of those resources to key fitness functions. This coordination of resource allocation relative to resource availability is commonly attributed to key nutrient sensing gene pathways in laboratory model organisms, chiefly the insulin/TOR signaling pathway. However, the genetic basis of diet-induced variation in gene expression is less clear.ResultsTo describe the natural genetic variation underlying nutrient-dependent differences, we used an outbred panel derived from a multiparental population, the Drosophila Synthetic Population Resource. We analyzed RNA sequence data from multiple female tissue samples dissected from flies reared in three nutritional conditions: high sugar (HS), dietary restriction (DR), and control (C) diets. A large proportion of genes in the experiment (19.6% or 2,471 genes) were significantly differentially expressed for the effect of diet, 7.8% (978 genes) for the effect of the interaction between diet and tissue type (LRT, Padj. < 0.05). Interestingly, we observed similar patterns of gene expression relative to the C diet, in the DR and HS treated flies, a response likely reflecting diet component ratios. Hierarchical clustering identified 21 robust gene modules showing intra-modularly similar patterns of expression across diets, all of which were highly significant for diet or diet-tissue interaction effects (false discovery rate, FDR Padj. < 0.05). Gene set enrichment analysis for different diet-tissue combinations revealed a diverse set of pathways and gene ontology (GO) terms (two-sample t-test, FDR < 0.05). GO analysis on individual co-expressed modules likewise showed a large number of terms encompassing a large number of cellular and nuclear processes (Fisher exact test, Padj. < 0.01). Although a handful of genes in the IIS/TOR pathway including Ilp5, Rheb, and Sirt2 showed significant elevation in expression, known key genes such as InR, chico, insulin peptide genes, and the nutrient-sensing pathways were not observed.ConclusionsOur results suggest that a more diverse network of pathways and gene networks mediate the diet response in our population. These results have important implications for future studies focusing on diet responses in natural populations.

Download Full-text

Drug screens of NGLY1 Deficiency worm and fly models reveal catecholamine, NRF2 and anti-inflammatory pathway activation as clinical approaches

10.1101/563478 ◽

2019 ◽

Author(s):

Sangeetha Iyer ◽

Joshua D. Mast ◽

Hillary Tsang ◽

Tamy P. Rodriguez ◽

Nina DiPrimio ◽

...

Keyword(s):

Human Cell ◽

Gene Networks ◽

Transcriptional Regulator ◽

Model Organisms ◽

Dopamine Receptor Agonist ◽

Lead Discovery ◽

Larval Size ◽

Toxic Dose ◽

Cellular Models ◽

Anti Inflammatory

AbstractN-glycanase 1/NGLY1 Deficiency is an ultra-rare and complex monogenic glycosylation disorder that affects fewer than 40 patients globally. NGLY1 Deficiency has been studied in model organisms such as yeast, worms, flies and mice. Proteasomal and mitochondrial homeostasis gene networks are controlled by the evolutionarily conserved transcriptional regulator Nrf1, whose activity requires deglycosylation by NGLY1. Hypersensitivity to the proteasome inhibitor bortezomib is a common phenotype observed in whole animal and cellular models of NGLY1 Deficiency. Here we describe unbiased phenotypic drug screens to identify FDA approved drugs, generally recognized as safe natural products and novel chemical entities that rescue growth and development of NGLY1-deficient worm and fly larvae treated with a toxic dose of bortezomib. We used image-based larval size and number assays for use in screens of a 2,560-member drug repurposing library and a 20,240-member lead discovery library. A total of 91 validated hit compounds from primary invertebrate screens were tested in a human cell line in a NRF2 activity assay. NRF2 is a transcriptional regulator that regulates cellular redox homeostasis and it can compensate for loss of Nrf1. Plant-based polyphenols comprise the largest class of hit compounds and NRF2 inducers. Catecholamines and catecholamine receptor activators comprise the second largest class of hits. Steroidal and non-steroidal anti-inflammatory drugs comprise the third largest class. Only one compound was active in all assays and species: the atypical antipsychotic and dopamine receptor agonist aripiprazole. Worm and fly models of NGLY1 Deficiency validate therapeutic rationales for activation of NRF2 and anti-inflammatory pathways based on results in mice and human cell models and suggest a novel therapeutic rationale for boosting catecholamine levels and/or signaling in the brain.

Download Full-text

Cross-species alcohol dependence-associated gene networks: Co-analysis of mouse brain gene expression and human genome-wide association data

10.1101/380584 ◽

2018 ◽

Author(s):

Kristin M. Mignogna ◽

Silviu A. Bacanu ◽

Brien P. Riley ◽

Aaron R. Wolen ◽

Michael F. Miles

Keyword(s):

Gene Expression ◽

Alcohol Dependence ◽

Mouse Brain ◽

Gene Networks ◽

Association Studies ◽

Complex Trait ◽

Genome Wide Association ◽

Model Organisms ◽

Genome Wide Association Studies ◽

Genome Wide

AbstractGenome-wide association studies on alcohol dependence, by themselves, have yet to account for the estimated heritability of the disorder and provide incomplete mechanistic understanding of this complex trait. Integrating brain ethanol-responsive gene expression networks from model organisms with human genetic data on alcohol dependence could aid in identifying dependence-associated genes and functional networks in which they are involved. This study used a modification of the Edge-Weighted Dense Module Searching for genome-wide association studies (EW-dmGWAS) approach to co-analyze whole-genome gene expression data from ethanol-exposed mouse brain tissue, human protein-protein interaction databases and alcohol dependence-related genome-wide association studies. Results revealed novel ethanol-regulated and alcohol dependence-associated gene networks in prefrontal cortex, nucleus accumbens, and ventral tegmental area. Three of these networks were overrepresented with genome-wide association signals from an independent dataset. These networks were significantly overrepresented for gene ontology categories involving several mechanisms, including actin filament-based activity, transcript regulation, Wnt and Syndecan-mediated signaling, and ubiquitination. Together, these studies provide novel insight for brain mechanisms contributing to alcohol dependence.

Download Full-text

Xenacoelomorpha Nervous Systems

Oxford Research Encyclopedia of Neuroscience ◽

10.1093/acrefore/9780190264086.013.203 ◽

2017 ◽

Cited By ~ 6

Author(s):

Pedro Martínez ◽

Volker Hartenstein ◽

Simon G. Sprecher

Keyword(s):

Gene Networks ◽

Parallel Evolution ◽

Evolutionary Process ◽

Morphological Characters ◽

Nervous Systems ◽

Transmission Electron ◽

Unique System ◽

Changing Roles ◽

History Of ◽

The Many

The emergence and diversification of bilateral animals are among the most important transitions in the history of life on our planet. A proper understanding of the evolutionary process will derive from answering such key questions as, how did complex body plans arise in evolutionary time, and how are complex body plans “encoded” in the genome? the first step is focusing on the earliest stages in bilaterian evolution, probing the most elusive organization of the genomes and microscopic anatomy in basally branching taxa, which are currently assembled in a clade named Xenacoelomorpha. This enigmatic phylum is composed of three major taxa: acoel flatworms, nemertodermatids, and xenoturbellids. Interestingly, the constituent species of this clade have an enormously varied set of morphologies; not just the obvious external features but also their tissues present a high degree of constructional variation. This interesting diversity of morphologies (a clear example being the nervous system, with animals showing different degrees of compaction) provides a unique system in which to address outstanding questions regarding the parallel evolution of genomes and the many morphological characters encoded by them. A systematic exploration of the anatomy of members of these three taxa, employing immunohistochemistry, in situ hybridization, and high-throughput transmission electron microscopy, will provide the reference framework necessary to understand the changing roles of genes and gene networks during the evolution of xenacoelomorph morphologies and, in particular, of their nervous systems.

Download Full-text

corseq: fast and efficient identification of favoured codons from next generation sequencing reads

PeerJ ◽

10.7717/peerj.5099 ◽

2018 ◽

Vol 6 ◽

pp. e5099 ◽

Cited By ~ 1

Author(s):

Salvatore Camiolo ◽

Andrea Porceddu

Keyword(s):

Genomic Sequence ◽

Gene Annotation ◽

Synonymous Codon ◽

Synonymous Codon Usage ◽

Model Organisms ◽

Coding Sequences ◽

Rnaseq Data ◽

Highly Expressed Genes ◽

Or Gene ◽

Generation Sequencing

Background Optimization of transgene expression can be achieved by designing coding sequences with the synonymous codon usage of genes which are highly expressed in the host organism. The identification of the so-called “favoured codons” generally requires the access to either the genome or the coding sequences and the availability of expression data. Results Here we describe corseq, a fast and reliable software for detecting the favoured codons directly from RNAseq data without prior knowledge of genomic sequence or gene annotation. The presented tool allows the inference of codons that are preferentially used in highly expressed genes while estimating the transcripts abundance by a new kmer based approach. corseq is implemented in Python and runs under any operating system. The software requires the Biopython 1.65 library (or later versions) and is available under the ‘GNU General Public License version 3’ at the project webpage https://sourceforge.net/projects/corseq/files. Conclusion corseq represents a faster and easy-to-use alternative for the detection of favoured codons in non model organisms.

Download Full-text