Reply to Jiang and Zhang: Parallel transcriptomic signature of monogamy: What is the null hypothesis anyway?

Young, Rebecca L.; Hofmann, Hans A.

doi:10.1073/pnas.1911022116

Cited by 3 publications

(5 citation statements)

References 10 publications

(6 reference statements)

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“…We identified 1626 and 1793 one-to-one orthologs for microarray and RNA-seq, respectively, consistent 206 with other comparative gene expression studies spanning vertebrates (Young et al, 2019). One-to-one 207 orthologs from microarray and RNA-seq datasets from the same species were largely non-overlapping.…”

Section: Variation In Gene Sets and Alignment Of Embryonic Stage Clussupporting

confidence: 79%

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Comparative transcriptomics reveal distinct patterns of gene expression conservation through vertebrate embryogenesis

Chan

Bhamidipati

Goldsby

et al. 2019

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15Despite the diversity of life, studies of variation across animals often remind us of our deep evolutionary 16 past. Abundant genome sequencing over the last ~25 years reveals remarkable conservation of genes and 17 recent analyses of gene regulatory networks illustrate that not only genes but entire pathways are conserved, 18 reused, and elaborated in the evolution of diversity. Predating these discoveries, 19 th -century embryologists 19 observed that though morphology at birth varies tremendously, certain stages of embryogenesis appear 20 remarkably similar across vertebrates. Specifically, while early and late stages are variable across species, 21 anatomy of mid-stages embryos (the phylotypic stage) is conserved. This model of vertebrate development 22

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Section: Variation In Gene Sets and Alignment Of Embryonic Stage Clussupporting

confidence: 79%

“…Finally, studies comparing gene expression similarity 268 across the transcriptome directly test against a null hypothesis. Such a test is critical because the degree of 269 variation expected through developmental stages across species is unknown (Young and Hofmann, 2019). 270…”

Section: Discussion 258mentioning

confidence: 99%

Comparative transcriptomics reveal distinct patterns of gene expression conservation through vertebrate embryogenesis

Chan

Bhamidipati

Goldsby

et al. 2019

Preprint

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“…Alternatively, selection of developmental stages or specific gene sets to compare may lead to different results and interpretations. Finally, studies that compare gene expression similarity at the transcriptome level rarely test against a null hypothesis ( Young and Hofmann 2019 ). Such a test is critical because the degree of variation expected through developmental stages across species is unknown ( Church and Extavour 2020 ).…”

Section: Discussionmentioning

confidence: 99%

“…However, how to identify the relevant gene set (i.e., kernel or ChIN) that is fundamental for shared developmental processes of vertebrate embryogenesis is unclear. Finally, it is often not clear what the appropriate null expectation should be in comparative studies, as it may depend on the type of data available and the level of analysis ( Dunn et al 2018 ; Young and Hofmann 2019 ; Church and Extavour 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomics Reveals Distinct Patterns of Gene Expression Conservation through Vertebrate Embryogenesis

Chan

Bhamidipati

Goldsby

et al. 2021

Genome Biology and Evolution

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Despite life’s diversity, studies of variation often remind us of our shared evolutionary past. Abundant genome sequencing and analyses of gene regulatory networks illustrate that genes and entire pathways are conserved, reused, and elaborated in the evolution of diversity. Predating these discoveries, 19th-century embryologists observed that though morphology at birth varies tremendously, certain stages of vertebrate embryogenesis appear remarkably similar across vertebrates. In the mid to late 20th century, anatomical variability of early and late stage embryos and conservation of mid-stages embryos (the ‘phylotypic’ stage) was named the hourglass model of diversification. This model has found mixed support in recent analyses comparing gene expression across species possibly owing to differences in species, embryonic stages, and gene sets compared. We compare 186 microarray and RNA-seq data sets covering embryogenesis in six vertebrate species. We use an unbiased clustering approach to group stages of embryogenesis by transcriptomic similarity and ask whether gene expression similarity of clustered embryonic stages deviates from a null expectation. We characterize expression conservation pattern of each gene at each evolutionary node after correcting for phylogenetic non-independence. We find significant enrichment of genes exhibiting early conservation, hourglass, late conservation patterns in both microarray and RNA-seq data sets. Enrichment of genes showing patterned conservation through embryogenesis indicates diversification of embryogenesis may be temporally constrained. However, the circumstances under which each pattern emerges remain unknown and require both broad evolutionary sampling and systematic examination of embryogenesis across species.

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“…Thus, evolutionary changes in temporal and spatial gene expression patterns (e.g., tissue or cell expression domains) over the course of ontogeny can result in the loss (addition) of genes from (into) existing gene co-expression networks, potentially influencing the phenotype (78, reviewed in: , 79). Finally, because like other complex traits, the transcriptome is shaped by stabilizing selection (80)(81)(82) and evolves via neutral or nearly neutral processes (e.g., drift; , 83), testing hypotheses of convergent evolution of phenotypes using transcriptomics data requires examination of differential expression and gene co-expression combined with rigorous phylogenetic comparative analyses and tests of appropriate null hypotheses (84,85). from six sympatric wrasse species that vary in mutualistic cleaning behavior including three noncleaning species, two facultative cleaning species, and one obligate cleaning species (Fig.…”

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Shared neural transcriptomic patterns underlie the repeated evolution of mutualistic cleaning behavior in Labridae wrasses

Young¹,

Weitekamp²,

Triki³

et al. 2022

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Despite the remarkable diversity of life forms on earth, evolutionary biologists have discovered numerous instances where even distantly related species share astonishing similarities in how they behave, look, and function. Given the importance of happenstance in evolution (e.g., random mutations, genetic drift, environmental stochasticity), it is often assumed that the mechanisms underlying such convergent phenotypes are distinct. Nevertheless, recent discoveries that the same pathways can underlie convergently evolved phenotypes have reinvigorated questions about the predictability of evolution and whether broadly conserved genomic mechanisms facilitate phenotypic convergence. Here, we generated transcriptomes of the putative teleost homologs of the mammalian hippocampus and basolateral amygdala, broadly associated with spatial and social cognition, in six sympatric species of Labridae wrasses that vary in mutualistic cleaning behavior (including three non-cleaning, two facultative cleaning, and one obligate cleaning species) and combined differential gene expression, gene co-expression, and phylogenetic comparative analyses to test two hypotheses about convergent evolution and specialization of mutualistic cleaning behavior. We first identify genes and gene modules exhibiting parallel neurotranscriptomic patterns in the repeated evolution of facultative cleaning. We then examined whether expression and co-expression patterns associated with facultative cleaning are also shared in the obligate cleaner species in our dataset and found evidence for transcriptomic concordance, though no evidence for additional specialization. Taken together, our results provide insights into the convergent evolution and the neuromolecular basis of cooperative behavior and, more generally, illustrate the potential of phylogenetic comparative transcriptomics to unravel the mechanistic underpinnings of the repeated evolution of complex organismal phenotypes.

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Reply to Jiang and Zhang: Parallel transcriptomic signature of monogamy: What is the null hypothesis anyway?

Cited by 3 publications

References 10 publications

Comparative transcriptomics reveal distinct patterns of gene expression conservation through vertebrate embryogenesis

Comparative transcriptomics reveal distinct patterns of gene expression conservation through vertebrate embryogenesis

Comparative Transcriptomics Reveals Distinct Patterns of Gene Expression Conservation through Vertebrate Embryogenesis

Shared neural transcriptomic patterns underlie the repeated evolution of mutualistic cleaning behavior in Labridae wrasses

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