Morphological and molecular evidence of cryptic speciation in sympatric colour morphotypes of Mycale (Carmia) cecilia (Porifera: Poecilosclerida) from the Mexican Pacific
DOI:
https://doi.org/10.3989/scimar.05339.082Keywords:
Porifera, anisochelae categories, cryptic species, COI, 28S rRNA, ITS1, colour morphotype, transcriptomicsAbstract
Identifying cryptic species is pivotal for understanding marine biodiversity and optimizing strategies for its conservation. A robust understanding of poriferan diversity is a complex endeavour. It has also been extremely hampered by the high phenotypic plasticity and the limited number of diagnostic characters. Mycale (Carmia) cecilia has different body colours, even among individuals living together. We tested whether the colour variation could be due to polymorphism, phenotypic plasticity or cryptic speciation. Phylogenetic reconstructions of nuclear and mitochondrial loci were congruent. Individuals of different body colour did not cluster together and had high levels of genetic divergence. Furthermore, the green morphotype clustered in almost all reconstructions with Mycale (C.) phyllophila, as both showed higher gene similarity at the transcriptomic level (public transcriptome). Morphologically, the green individuals consistently showed discrepancies from the red ones. These results suggest that all individuals with the same body colour, either red or green, correspond to the same species, while individuals with different body colours probably belong to different species. These results reveal high levels of morphologic and genetic diversity, which could have important implications for what is known as M. (C.) cecilia and the Mycalidae systematics.
Downloads
References
Adlard R., Lester R.J. 1995. Development of a diagnostic test for Mikrocytos roughleyi, the aetiological agent of Australian winter mortality of the commercial rock oyster, Saccostrea commercialis (Iredale and Roughley). J. Fish Dis. 18: 609-614. https://doi.org/10.1111/j.1365-2761.1995.tb00365.x
Becking L.E., Erpenbeck D., Peijnenburg K.T.C.A., de Voogd N.J. 2013. Phylogeography of the Sponge Suberites diversicolor in Indonesia: Insights into the Evolution of Marine Lake Populations. PLoS ONE 8: e75996. https://doi.org/10.1371/journal.pone.0075996 PMid:24098416 PMCid:PMC3788070
Belinky F., Szitenberg A., Goldfarb I., et al. 2012. ALG11 - A new variable DNA marker for sponge phylogeny: Comparison of phylogenetic performances with the 18S rDNA and the COI gene. Mol. Phylogenet. Evol. 63: 702-713. https://doi.org/10.1016/j.ympev.2012.02.008 PMid:22387211
Bickford D., Lohman D.J., Sodhi N.S., Ng P.KL., Meier R., Winker K., Ingram KK., Das I. 2006. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148-155. https://doi.org/10.1016/j.tree.2006.11.004 PMid:17129636
Blanquer A., Uriz M-J. 2007. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: A phylogenetic approach. Mol. Phylogenet. Evol. 45: 392-397. https://doi.org/10.1016/j.ympev.2007.03.004 PMid:17434762
Blanquer A., Uriz M-J. 2008. "A posteriori" searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Dictyonellidae: Scopalina). Invertebr. Syst. 22: 489-502. https://doi.org/10.1071/IS07004 https://doi.org/10.1071/IS07004
Borchiellini C., Chombard C., Lafay B. NB-E. 2000. Molecular systematics of sponges (Porifera). Hydrobiologia. 420: 15-27. https://doi.org/10.1007/978-94-017-2184-4_2 https://doi.org/10.1007/978-94-017-2184-4_2
Bucklin A., Steinke D., Blanco-Bercial L. 2011. DNA Barcoding of Marine Metazoa. Ann. Rev. Mar. Sci. 3: 471-508. https://doi.org/10.1146/annurev-marine-120308-080950 https://doi.org/10.1146/annurev-marine-120308-080950 PMid:21329214
Carballo J.L., Cruz-Barraza J.A. 2008. First record of Axinyssa Lendenfeld, 1897 (Demospongiae, Halichondrida) from the East Pacific Ocean, with the description of Axinyssa isabela sp. nov. Zootaxa. 1784: 58-68. https://doi.org/10.11646/zootaxa.1784.1.4
Carballo J.L., Cruz-Barraza J.A. 2010. A revision of the genus Mycale (Poecilosclerida: Mycalidae) from the Mexican Pacific Ocean. Contrib. Zool. 79: 165-191. https://doi.org/10.1163/18759866-07904003
Cárdenas P., Pérez T., Boury-Esnault N. 2012. Sponge Systematics Facing New Challenges. Adv. Mar. Biol. 61: 79-209. https://doi.org/10.1016/B978-0-12-387787-1.00010-6 PMid:22560778
Cárdenas P., Rapp H.T., Schander C., Tendal O.S. 2010. Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) - Combining phylogenetic and Linnaean classification. Zool. Sci. 39: 89-106. https://doi.org/10.1111/j.1463-6409.2009.00402.x
Castillo-Páez A.Y., Llera-Herrera R., Cruz-Barraza J.A. 2021. De novo transcriptome assembly for two colour types of the marine sponge Mycale (Carmia) cecilia. Mol. Biol. Rep. 48: 1-4. https://doi.org/10.1007/s11033-021-06274-4 PMid:33782784
Chenauil A., Cahill A.E., Délémontey N., et al. 2019. Problems and questions posed by cryptic species. A framework to guide future studies. In: Casetta J., da Silva., Vecchi D. (eds), From Assessing to Conserving Biodiversity: Conceptual and Practical Challenges, pp. 77-106. https://doi.org/10.1007/978-3-030-10991-2_4
Desqueyroux-Faúndez R., van Soest R.W.M. 1997. Shallow waters Demosponges of the Galápagos Islands. Rev. Suisse Zool. 104: 379-467. https://doi.org/10.5962/bhl.part.80003
Emms D.M., Kelly S. 2017. STRIDE: Species Tree Root Inference from Gene Duplication Events. Mol. Biol. Evol. 34: 3267-3278. https://doi.org/10.1093/molbev/msx259 PMid:29029342 PMCid:PMC5850722
Emms D.M., Kelly S. 2018. STAG: Species Tree Inference from All Genes. BioRxiv. 267914. https://doi.org/10.1101/267914
Emms D.M., Kelly S. 2019. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20: 1-14. https://doi.org/10.1186/s13059-019-1832-y PMid:31727128 PMCid:PMC6857279
Escobar D., Zea S., Sánchez J.A. 2012. Phylogenetic relationships among the Caribbean members of the Cliona viridis complex (Porifera, Demospongiae, Hadromerida) using nuclear and mitochondrial DNA sequences. Mol. Phylogenet. Evol. 64: 271-284. https://doi.org/10.1016/j.ympev.2012.03.021 PMid:22510309
Esteves E.L., de Paula T.S., Lerner C., et al. 2018. Morphological and molecular systematics of the "Monanchora arbuscula complex" (Poecilosclerida: Crambeidae), with the description of five new species and a biogeographic discussion of the genus in the Tropical Western Atlantic. Invertebr. Syst. 32: 457-503. https://doi.org/10.1071/IS16088
Fusco G., Minelli A. 2010. Phenotypic plasticity in development and evolution: facts and concepts. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365: 547-556. https://doi.org/10.1098/rstb.2009.0267 PMid:20083631 PMCid:PMC2817147
Green G., Gómez P. 1985. Estudio taxonómico de las esponjas de la Bahía de Mazatlán Sinaloa, México. An. Cent. Cienc. Mar. Limnol. 273-300.
Haas B.J., Papanicolaou A., Yassour M., et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8: 1494-1512. https://doi.org/10.1038/nprot.2013.084 PMid:23845962 PMCid:PMC3875132
Hajdu E., Riitzler K. 1998. Sponges, genus Mycale (Poecilosclerida: Demospongiae: Porifera), from a Caribbean mangrove and comments on subgeneric classification. Proc. Biol. Soc. Wash. 111: 737-773.
Huang D., Meier R., Todd P.A., Chou L.M. 2008. Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J. Mol. Evol. 66: 167-174. https://doi.org/10.1007/s00239-008-9069-5 PMid:18259800
Kenny N.J., Itskovich V.B. 2020. Phylogenomic inference of the interrelationships of Lake Baikal sponges. Syst. Biodivers. 0: 1-9.
Knapp I.S., Forsman Z.H., Williams G.J., et al. 2015. Cryptic species obscure introduction pathway of the blue Caribbean sponge (Haliclona (Soestella) caerulea), (order: Haplosclerida) to Palmyra Atoll, Central Pacific. PeerJ. 2015. https://doi.org/10.7717/peerj.1170 https://doi.org/10.7717/peerj.1170 PMid:26339548 PMCid:PMC4558080
Knowlton N. 1993. Sibling species in the sea. Annu. Rev. Ecol. Syst. 24: 189-216. https://doi.org/10.1146/annurev.es.24.110193.001201 https://doi.org/10.1146/annurev.es.24.110193.001201
Kumar S., Stecher G., Li M., et al. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549. https://doi.org/10.1093/molbev/msy096 PMid:29722887 PMCid:PMC5967553
de Laubenfels M.W. 1936. A comparison of the shallow-water sponges near The Pacific and of The Panama Canal with those at The Caribbean end. Proc U. S. Natl. Mus. 83: 441-466. https://doi.org/10.5479/si.00963801.83-2993.441
de Laubenfels M.W. 1950. The sponges of Kaneohe Bay, Oahu. Pac. Sci. 4: 3-36.
Loh T.L., López-Legentil S., Song B., Pawlik J.R. 2012. Phenotypic variability in the Caribbean Orange Icing sponge Mycale laevis (Demospongiae: Poecilosclerida). Hydrobiologia. 687: 205-217. https://doi.org/10.1007/s10750-011-0806-1
López-Legentil S., Erwin P.M., Henkel T.P., et al. 2010. Phenotypic plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida). Sci. Mar. 74: 445-453. https://doi.org/10.3989/scimar.2010.74n3445
Ortega M.J., Zubía E., Sánchez M.C., et al. 2004. Structure and cytotoxicity of new metabolites from the sponge Mycale cecilia. Tetrahedron. 60: 251-2524. https://doi.org/10.1016/j.tet.2004.01.056
Park M-H.H., Sim C-J.J., Baek J., Min G-S.S. 2007. Identification of genes suitable for DNA barcoding of morphologically indistinguishable Korean Halichondriidae sponges. Mol. Cells. 23: 220-227. https://doi.org/10.1016/S1016-8478(23)07377-6 PMid:17464200
Petit R.J., Excoffier L. 2009. Gene flow and species delimitation. Trends Ecol. Evol. 24: 386-393. https://doi.org/10.1016/j.tree.2009.02.011 PMid:19409650
Pfenninger M., Schwenk K. 2007. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC. Evol. Biol. 7: 1-6. https://doi.org/10.1186/1471-2148-7-121 PMid:17640383 PMCid:PMC1939701
Puillandre N., Brouillet S., Achaz G. 2021. ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21: 609-620. https://doi.org/10.1111/1755-0998.13281 PMid:33058550
De Queiroz K. 2007. Species concepts and species delimitation. Syst. Biol. 56: 879-886. https://doi.org/10.1080/10635150701701083 PMid:18027281
Shaffer M.R., Davy SK., Bell J.J. 2019. Hidden diversity in the genus Tethya: comparing molecular and morphological techniques for species identification. Heredity. 122: 354-369. https://doi.org/10.1038/s41437-018-0134-6 PMid:30131516 PMCid:PMC6460755
Van Soest R.W.M.M., Hajdu E. 2002. Family Mycalidae Lundbeck, 1905. In: Hooper J.N.A., Van Soest R.W.M. (eds), Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York, pp. 669-690. https://doi.org/10.1007/978-1-4615-0747-5_73
Uriz M.J., Turon X. 2012. Sponge ecology in the molecular era. Adv. Mar. Biol. 61: 345-410. https://doi.org/10.1016/B978-0-12-387787-1.00006-4 PMid:22560781
Uriz M.J., Garate L., Agell G. 2017. Molecular phylogenies confirm the presence of two cryptic Hemimycale species in the mediterranean and reveal the polyphyly of the genera Crella and Hemimycale (Demospongiae: Poecilosclerida). PeerJ 5:e2958. https://doi.org/10.7717/peerj.2958 PMid:28286707 PMCid:PMC5344016
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.
Funding data
Universidad Nacional Autónoma de México
Grant numbers PAPIIT-UNAM IN210018
