Evolutionary loss of melanogenesis in the tunicate Molgula occulta

Claudia Racioppi, Maria Carmen Valoroso, Ugo Coppola, Elijah K. Lowe, C. Titus Brown, Billie J. Swalla, Lionel Christiaen, Alberto Stolfi, Filomena Ristoratore

Research output: Contribution to journalArticle

Abstract

Background: Analyzing close species with diverse developmental modes is instrumental for investigating the evolutionary significance 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 different alleles independently acquired frameshifting 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 interspecific 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.

Original languageEnglish (US)
Article number11
JournalEvoDevo
Volume8
Issue number1
DOIs
StatePublished - Jul 18 2017

Fingerprint

Molgula
Molgula oculata
melanogenesis
Urochordata
Monophenol Monooxygenase
Tunicata
melanocytes
pseudogenes
gene
pigment
embryo
embryo (animal)
sense organs
pigments
larva
Molgulidae
larvae
Pseudogenes
allele
vertebrate

Keywords

  • Phylogeny
  • Pigmentation
  • Pseudogenes
  • Transposable elements
  • Tyrosinase evolution

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Developmental Biology

Cite this

Racioppi, C., Valoroso, M. C., Coppola, U., Lowe, E. K., Brown, C. T., Swalla, B. J., ... Ristoratore, F. (2017). Evolutionary loss of melanogenesis in the tunicate Molgula occulta. EvoDevo, 8(1), [11]. https://doi.org/10.1186/s13227-017-0074-x

Evolutionary loss of melanogenesis in the tunicate Molgula occulta. / Racioppi, Claudia; Valoroso, Maria Carmen; Coppola, Ugo; Lowe, Elijah K.; Brown, C. Titus; Swalla, Billie J.; Christiaen, Lionel; Stolfi, Alberto; Ristoratore, Filomena.

In: EvoDevo, Vol. 8, No. 1, 11, 18.07.2017.

Research output: Contribution to journalArticle

Racioppi, C, Valoroso, MC, Coppola, U, Lowe, EK, Brown, CT, Swalla, BJ, Christiaen, L, Stolfi, A & Ristoratore, F 2017, 'Evolutionary loss of melanogenesis in the tunicate Molgula occulta', EvoDevo, vol. 8, no. 1, 11. https://doi.org/10.1186/s13227-017-0074-x
Racioppi C, Valoroso MC, Coppola U, Lowe EK, Brown CT, Swalla BJ et al. Evolutionary loss of melanogenesis in the tunicate Molgula occulta. EvoDevo. 2017 Jul 18;8(1). 11. https://doi.org/10.1186/s13227-017-0074-x
Racioppi, Claudia ; Valoroso, Maria Carmen ; Coppola, Ugo ; Lowe, Elijah K. ; Brown, C. Titus ; Swalla, Billie J. ; Christiaen, Lionel ; Stolfi, Alberto ; Ristoratore, Filomena. / Evolutionary loss of melanogenesis in the tunicate Molgula occulta. In: EvoDevo. 2017 ; Vol. 8, No. 1.
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AU - Racioppi, Claudia

AU - Valoroso, Maria Carmen

AU - Coppola, Ugo

AU - Lowe, Elijah K.

AU - Brown, C. Titus

AU - Swalla, Billie J.

AU - Christiaen, Lionel

AU - Stolfi, Alberto

AU - Ristoratore, Filomena

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N2 - Background: Analyzing close species with diverse developmental modes is instrumental for investigating the evolutionary significance 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 different alleles independently acquired frameshifting 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 interspecific 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.

AB - Background: Analyzing close species with diverse developmental modes is instrumental for investigating the evolutionary significance 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 different alleles independently acquired frameshifting 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 interspecific 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.

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KW - Pseudogenes

KW - Transposable elements

KW - Tyrosinase evolution

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