Differential Expression in Testis and Liver Transcriptomes from Four Species of Peromyscus (Rodentia: Cricetidae).

Caleb D Phillips,David A Ray,Roy N Platt,Ellen Pritham,Robert D Bradley,Laramie L Lindsey

doi:10.1093/gbe/evz280

Abstract

The genus Peromyscus represents a rapidly diverged clade of Cricetid rodents that contains multiple cryptic species and has a propensity for morphologic conservation across its members. The unresolved relationships in previously proposed phylogenies reflect a suspected rapid adaptive radiation. To identify functional groups of genes that may be important in reproductive isolation in a reoccurring fashion across the Peromyscus phylogeny, liver and testis transcriptomes from four species (P. attwateri, P. boylii, P. leucopus, and P. maniculatus) were generated and differential expression (DE) tests were conducted. Taxa were selected to represent members diverged from a common ancestor: P. attwateri + P. boylii (clade A), and P. leucopus + P. maniculatus (clade B). Comparison of clades (A vs. B) suggested that 252 transcripts had significant DE in the liver data set, whereas significant DE was identified for 657 transcripts in the testis data set. Further, 45 genes had DE isoforms in the 657 testis transcripts and most of these functioned in major reproductive roles such as acrosome assembly, spermatogenesis, and cell cycle processes (meiosis). DE transcripts in the liver mapped to more broad gene ontology terms (metabolic processes, catabolic processes, response to chemical, and regulatory processes), and DE transcripts in the testis mapped to gene ontology terms associated with reproductive processes, such as meiosis, sperm motility, acrosome assembly, and sperm–egg fusion. These results suggest that a suite of genes that conduct similar functions in the testes may be responsible for the adaptive radiation events and potential reoccurring speciation of Peromyscus in terms of reproduction through varying expression levels.

Highlights

Nascent species resulting from adaptive radiations often display substantive morphological differences (Losos and Miles 2002); structural and functional genomic changes may facilitate adaptive divergence without overt morphological differences (Kirkpatrick and Barton 2006; Rowe et al 2011)
differential expression (DE) transcripts in the liver mapped to more broad gene ontology terms, and DE transcripts in the testis mapped to gene ontology terms associated with reproductive processes, such as meiosis, sperm motility, acrosome assembly, and sperm–egg fusion
Differential expression (DE) studies have been conducted on Peromyscus to determine how variations in gene expression contribute to challenging environments, behavioral characteristics of Peromyscus, and mating systems; to date, no studies have examined the effects of gene expression patterns on potential mode(s) of speciation of the group

Summary

Introduction

Nascent species resulting from adaptive radiations often display substantive morphological differences (Losos and Miles 2002); structural and functional genomic changes may facilitate adaptive divergence without overt morphological differences (Kirkpatrick and Barton 2006; Rowe et al 2011). Differential expression (DE) studies have been conducted on Peromyscus to determine how variations in gene expression contribute to challenging environments, behavioral characteristics of Peromyscus, and mating systems (all reviewed by Munshi-South and Richardson [2017]); to date, no studies have examined the effects of gene expression patterns on potential mode(s) of speciation of the group. Gene expression plays a significant role in evolutionary processes and speciation (Galili et al 1988; Pfennig et al 2010); many obstacles exist to fully understand this phenomenon including technological restrictions (Wolf et al 2010). Some researchers have been able to quantitatively examine DE in relation to speciation.

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