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'Seahorse Brood Pouch Transcriptome Reveals Common Genes Associated View metadata, citation and similar papers at core.ac.uk brought to you by CORE Seahorse Brood Pouch Transcriptome Reveals Commonprovided Genes by RERO DOC Digital Library Associated with Vertebrate Pregnancy Camilla M. Whittington,*,1,2 Oliver W. Griffith,2 Weihong Qi,3 Michael B. Thompson,2 and Anthony B. Wilson*,1,4,5 1Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland 2School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia 3Functional Genomics Centre, University of Zurich, Zurich, Switzerland 4Department of Biology, Brooklyn College 5The Graduate Center, City University of New York *Corresponding author: E-mail: [email protected]; [email protected]. Associate editor: Gunter Wagner Abstract Viviparity (live birth) has evolved more than 150 times in vertebrates, and represents an excellent model system for studying the evolution of complex traits. There are at least 23 independent origins of viviparity in fishes, with syngnathid fishes (seahorses and pipefish) unique in exhibiting male pregnancy. Male seahorses and pipefish have evolved specialized brooding pouches that provide protection, gas exchange, osmoregulation, and limited nutrient provisioning to devel- oping embryos. Pouch structures differ widely across the Syngnathidae, offering an ideal opportunity to study the evolution of reproductive complexity. However, the physiological and genetic changes facilitating male pregnancy are largely unknown. We used transcriptome profiling to examine pouch gene expression at successive gestational stages in a syngnathid with the most complex brood pouch morphology, the seahorse Hippocampus abdominalis. Using a unique time-calibrated RNA-seq data set including brood pouch at key stages of embryonic development, we identified transcriptional changes associated with brood pouch remodeling, nutrient and waste transport, gas exchange, osmoreg- ulation, and immunological protection of developing embryos at conception, development and parturition. Key seahorse transcripts share homology with genes of reproductive functioninpregnantmammals,reptiles, and other live-bearing fish, suggesting a common toolkit of genes regulating pregnancy in divergent evolutionary lineages. Key words: brood pouch, evolution, gestation, Hippocampus abdominalis, live birth, male pregnancy, reproduction, RNA-seq, Syngnathidae. Introduction every major vertebrate lineage, including at least 23 times in Article The evolution of novel traits is underpinned by genetic fishes (Blackburn 2015). The repeated origin of viviparity by changes that encode new phenotypes. The genetic basis of convergent evolution offers the opportunity to examine in- phenotypic traits that are controlled by few genes is well dependent evolutionary origins of reproductive complexity known. For example, mosquitoes with a regulatory mutation and to uncover the processes by which viviparity evolves at in the gene encoding a single enzyme are insecticide resistant the genetic level. (Mitchell et al. 2012), and mutations in the Melanocortin 1 Syngnathid fishes (seahorses, pipefishes, and seadragons), a receptor gene influence coat color in animals ranging from family of approximately 300 species, represent the only mice (e.g., Hoekstra et al. 2006)tomammoths(Rompler€ et al. known examples of male pregnant animals (Stolting and 2006). In contrast, we know little about the genetic basis of Wilson 2007). The syngnathid brood pouch, derived from complex traits that have resulted from changes in many abdominal epithelium, is functionally equivalent to the am- genes, which have proven difficult to study using traditional niote (mammal and reptile) uterus. Females transfer large, genetic methods. Recent developments in deep sequencing yolk-rich eggs into the pouch, which the male immediately technologies (RNA-seq) facilitate the examination of net- fertilizes, assuring their paternity (Van Look et al. 2007). The works of genes responsible for the evolution of complex phe- complexity of the syngnathid brood pouch varies across the notypes. Viviparity (live birth) is one such trait, a highly family (ranging from simple egg attachment sites through to developed form of reproduction requiring the evolution of the fleshy, fully enclosed brood pouch of seahorses), repre- a diverse set of adaptations involved in regulating the internal senting an excellent system in which to explore the evolution reproductive environment and provisioning developing em- of reproductive complexity (Wilson et al. 2003; Wilson and bryos inside the parent. Viviparity has evolved from oviparity Orr 2011). However, despite the important role of this group (egg laying) independently at least 150 times, across nearly as an evolutionary model of sexual selection (Rosenqvist and ß The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: [email protected] 3114 Mol. Biol. Evol. 32(12):3114–3131 doi:10.1093/molbev/msv177 Advance Access publication September 1, 2015 Seahorse Brood Pouch Transcriptome . doi:10.1093/molbev/msv177 MBE Berglund 2011), and widespread interest in the evolution of 2006; Small et al. 2013), but these studies have involved the viviparity (Blackburn 2015), the genetic, physiological and en- pooling of tissue between multiple individuals and reproduc- docrinological regulation of this unique form of reproduction tive stages, limiting the potential for associating transcrip- remain poorly understood (Stolting and Wilson 2007; Scobell tional changes with specific morphological restructuring and MacKenzie 2011). and physiological processes occurring during gestation. During gestation, the brood pouch undergoes significant Here we use deep sequencing technologies to examine morphological changes, including thickening, vascularization, changes in pouch gene expression during pregnancy in the development of epithelial microridges, and restructuring, as seahorse (Hippocampus abdominalis), a species exhibiting the embryos embed into the pouch epithelium (Carcupino et al. most complex form of male pregnancy. Using an RNA-seq 2002, 1997; Laksanawimol et al. 2006), morphological changes analysis of gene expression across multiple stages of preg- that parallel the restructuring of mammalian and reptilian nancy, we identify transcribed genes associated with crucial uteri during pregnancy (Renfree 2010; Murphy and biological processes in the pregnant pouch through key stages Thompson 2011). Although syngnathids lack the complex of conception, development, and parturition. Although pre- interdigitated placental structure found in mammals and vious studies have identified gene expression differences some reptiles (Oconer and Herrera 2003), there is evidence during pregnancy using microarrays (Knox and Baker 2008), of a pseudoplacenta in some species (Stolting and Wilson this is the first time that next-generation sequencing has been 2007), and the pregnant seahorse brood pouch epithelium used across the full range of pregnancy in any animal, pro- conforms to the widely accepted definition of a placenta as an viding a uniquely fine-scale view of gene expression changes “apposition or fusion of fetal membranes to the uterine associated with reproductive function. We identify a diverse mucosa for physiological exchange” (Mossman 1937), with range of transcripts differentially expressed across pregnancy the pouch epithelium being functionally equivalent to the that are associated with known physiological functions of the mucosal lining of the uterus. Brood pouch physiology differs seahorse brood pouch, a complex and uniquely derived re- among syngnathids, and pouch ultrastructure and function productive organ. vary even among pouches of closely related species The evolution of live birth requires a complex set of adap- (Carcupino et al. 2002; Ripley and Foran 2006), suggesting tations associated with embryonic development in a closed that pouch function can evolve rapidly following divergence. environment, including gas exchange, waste removal/storage, However, some pouch activities appear to be conserved and nutrient transport to the developing embryo. The differ- across taxa, including mechanical protection from predation entialexpressionofgenesassociatedwithsuchfunctionsmay and immunoprotection (Melamed et al. 2005; Roth et al. be facilitated through a number of mechanisms, including the 2012). The brood pouch also functions in gas exchange and pre-existing expression of transcripts in homologous tissues of waste removal, as well as osmoregulation (Linton and Soloff a nonviviparous ancestor, the recruitment of genes into new 1964; Quast and Howe 1980; Azzarello 1991; Watanabe et al. expression domains in derived reproductive tissues, and/or 1999; Ripley 2009). the evolution of novel reproductive genes through mutation A major innovation in the evolution of viviparity is matro- and/or gene duplication (True and Carroll 2002). We aimed trophy, the ability of mothers to provide supplementary nu- to identify whether common genes are associated with preg- trition to embryos during development. Evidence to support nancy in seahorses and other vertebrates. To this end, we apatrotrophicfunction(i.e.,supplementary nutrition from compare differentially expressed genes associated with repro- the father) of the syngnathid brood pouch is mixed, and ductive function in the seahorse brood pouch with genes pouch complexity does not necessarily
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