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Evolutionary Loss of Melanogenesis in the Tunicate Molgula Occulta Claudia Racioppi1,2,3, Maria Carmen Valoroso1,8, Ugo Coppola1, Elijah K

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Evolutionary Loss of Melanogenesis in the Tunicate Molgula Occulta Claudia Racioppi1,2,3, Maria Carmen Valoroso1,8, Ugo Coppola1, Elijah K Racioppi et al. EvoDevo (2017) 8:11 DOI 10.1186/s13227-017-0074-x EvoDevo RESEARCH Open Access Evolutionary loss of melanogenesis in the tunicate Molgula occulta Claudia Racioppi1,2,3, Maria Carmen Valoroso1,8, Ugo Coppola1, Elijah K. Lowe1,3,4,5, C. Titus Brown3,5,6, Billie J. Swalla3,4,5, Lionel Christiaen2,3, Alberto Stolf2,3,7* and Filomena Ristoratore1* Abstract Background: Analyzing close species with diverse developmental modes is instrumental for investigating the evolutionary signifcance of physiological, anatomical and behavioral features at a molecular level. Many examples of trait loss are known in metazoan populations living in dark environments. Tunicates are the closest living relatives of vertebrates and typically present a lifecycle with distinct motile larval and sessile adult stages. The nervous system of the motile larva contains melanized cells associated with geotactic and light-sensing organs. It has been suggested that these are homologous to vertebrate neural crest-derived melanocytes. Probably due to ecological adaptation to distinct habitats, several species of tunicates in the Molgulidae family have tailless (anural) larvae that fail to develop sensory organ-associated melanocytes. Here we studied the evolution of Tyrosinase family genes, indispensible for melanogenesis, in the anural, unpigmented Molgula occulta and in the tailed, pigmented Molgula oculata by using phylogenetic, developmental and molecular approaches. Results: We performed an evolutionary reconstruction of the tunicate Tyrosinase gene family: in particular, we found that M. oculata possesses genes predicted to encode one Tyrosinase (Tyr) and three Tyrosinase-related proteins (Tyrps) while M. occulta has only Tyr and Tyrp.a pseudogenes that are not likely to encode functional proteins. Analysis of Tyr sequences from various M. occulta individuals indicates that diferent alleles independently acquired frameshift- ing short indels and/or larger mobile genetic element insertions, resulting in pseudogenization of the Tyr locus. In M. oculata, Tyr is expressed in presumptive pigment cell precursors as in the model tunicate Ciona robusta. Furthermore, a M. oculata Tyr reporter gene construct was active in the pigment cell precursors of C. robusta embryos, hinting at conservation of the regulatory network underlying Tyr expression in tunicates. In contrast, we did not observe any expression of the Tyr pseudogene in M. occulta embryos. Similarly, M. occulta Tyr allele expression was not rescued in pigmented interspecifc M. occulta M. oculata hybrid embryos, suggesting deleterious mutations also to its cis- regulatory sequences. However, in ×situ hybridization for transcripts from the M. occulta Tyrp.a pseudogene revealed its expression in vestigial pigment cell precursors in this species. Conclusions: We reveal a complex evolutionary history of the melanogenesis pathway in tunicates, characterized by distinct gene duplication and loss events. Our expression and molecular data support a tight correlation between pseudogenization of Tyrosinase family members and the absence of pigmentation in the immotile larvae of M. occulta. These results suggest that relaxation of purifying selection has resulted in the loss of sensory organ-associated melanocytes and core genes in the melanogenesis biosynthetic pathway in M. occulta. Keywords: Pigmentation, Tyrosinase evolution, Transposable elements, Pseudogenes, Phylogeny *Correspondence: [email protected]; [email protected] 1 Biology and Evolution of Marine organisms, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy 2 Center for Developmental Genetics, Department of Biology, New York University, New York, NY, USA Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Racioppi et al. EvoDevo (2017) 8:11 Page 2 of 11 Background pseudogenized by deletions, insertions and codon sub- Closely related species with diferent modes of develop- stitutions in coding and noncoding regions, resulting in ment are attractive systems to investigate the molecular truncated proteins and/or reduced transcriptional activ- bases of evolutionary changes. Te evolutionary loss of ity [29, 30]. However, tail muscles are still specifed in physiological, anatomical and behavioral traits by cave- anural embryos, which express the same regulatory cas- dwelling animals is one noteworthy example [1]. For cade for myogenesis in tailed species [31, 32]. Similarly, instance, several studies have revealed convergent or anural embryos also specify notochord cells, but these parallel evolution of loss of pigmentation, eyes and vari- later fail to undergo proper morphogenesis by conver- ous behavioral adaptations in various populations of the gent extension [33]. Mexican cave tetra (Astyanax mexicanus), which have In contrast the loss of functional muscles and noto- evolved in parallel from surface-dwelling populations [2– chord, the loss of diferentiated neural structures in 4]. Insights into similar processes in cave-dwelling crus- anural larvae has not been studied in detail. Te most taceans are beginning to emerge [5]. obvious evolutionary loss of a neural structure is that of Tunicates are the sister group to the vertebrates and the sensory pigment cells, or melanocytes. While tuni- are characterized by a life cycle with distinct motile lar- cate larvae generally possess both an ocellus and otolith, val and sessile adult stages [6, 7]. Te tailed, tadpole-type most molgulids have only an otolith. Tey have lost the larva of a typical tunicate consists of a head containing ocellus and, concomitantly, the ability to respond to light a brain, and a tail containing a dorsal nerve cord and a [34]. In Molgula species with anural larvae, there has notochord fanked by striated muscle cells. Larvae swim been a more complete loss of pigmentation, as even the by alternated left–right contractions of the tail muscles, otolith is missing [19] or vestigial [26]. Tis has been pos- which are controlled by a minimal central nervous sys- tulated to be due the lack of adaptive value of the otolith tem containing only 177 neurons [8]. Inside the brain, for such anural larvae, which do not swim and therefore two sensory organs containing a single melanocyte each do not need to sense their orientation in the water col- are generally present: the otolith, for gravity perception, umn as swimming, tailed larvae do [22]. and the ocellus, for the detection of light [9, 10]. Tese Here we describe the development of sensory pigment two distinct pigment cells develop from a single bilateral cells in the embryos of Molgula oculata, and the molecu- pair of cells along the neural plate borders [11] and are lar basis of pigmentation loss in the closely related, anu- proposed to be homologous to pigment cells of the dorsal ral and unpigmented species M. occulta. We found that ocelli in amphioxus [12, 13] and to neural crest-derived inactivated Tyrosinase (Tyr) and Tyrosinase-related pro- melanocytes in vertebrates [14, 15]. Pigmentation in tein (Tyrp) genes are present in the genome of M. occulta, tunicates depends critically on the activity of melano- but are not likely to produce functional enzymes. While genic enzymes Tyrosinase (Tyr) and Tyrosinase-related Tyr transcripts were not detected in M. occulta embryos, proteins (Tyrps) [16, 17], as is the case in vertebrates [18]. transcription of a Tyrp gene was observed in vestig- Despite the deeply conserved body plan of the swim- ial pigment cells. Surprisingly, more than two distinct ming tunicate larva, some species instead develop a tail- Tyrosinase alleles with diferent inactivating mutations less (anural) larva which is immotile [19–21]. About 20 were cloned from a sampling of M. occulta individuals, tunicate species have been shown to exhibit anural devel- suggesting parallel loss of pigmentation by independent opment, and almost all of these species are members of loss-of-function mutations Tyrosinase within the same the family Molgulidae, in which tail loss has occurred population. independently multiple times [21, 22]. Te ecological sig- nifcance of these losses is still not clear, although it has Results been suggested that this could be related to the habitats Tyrosinase family enzymes in Molgula to which these species are adapted, notably sand fats and Te melanogenic toolkit of tunicates and vertebrates rocky shores at higher latitudes [22]. revolves around Tyrosinase family gene members, which Anural tunicate larvae have conspicuously lost most of encode the rate-limiting enzymes that catalyze the fnal those features more directly associated with swimming. steps in melanin biosynthesis [16]. In Ciona spp., the For instance, they have lost the ability to generate dif- family is comprised by Tyrosinase (Tyr), Tyrosinase- ferentiated tail muscles [23–28], and produce rounded related protein a (Tyrp.a) and Tyrosinase-related pro- larvae without the characteristic
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