First molecular phylogeny of Laevicaudata (Crustacea: Branchiopoda) with description of a new species of Lynceus from Chile and an updated key to species in the Americas
Zandra M. S. Sigvardt A H , D. Christopher Rogers B , Patricio De los Ríos C D , Ferran Palero E F G and Jørgen Olesen AA Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen Ø, Denmark.
B Kansas Biological Survey and the Natural History Museum (Biodiversity Institute), Kansas University, Higuchi Hall, 2101 Constant Avenue, Lawrence, KS 66047-3759, USA.
C Departamento de Ciencias Biológicas y Químicas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Casilla 15-D, Temuco, Chile.
D Núcleo de Estudios Ambientales, Universidad Católica de Temuco, Casilla 15-D, Temuco, Chile.
E Centre d’Estudis Avançats de Blanes (CEAB-CSIC), Carrer d’Accés a la Cala Sant Francesc 14, 17300 Blanes, Spain.
F Department of Invertebrate Zoology and Hydrobiology, Faculty of Biology and Environmental Protection, University of Łódź, ul. Banacha 12/16, 90-237 Łódź, Poland.
G Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.
H Corresponding author. Email: zandra@snm.ku.dk
Invertebrate Systematics 33(4) 597-617 https://doi.org/10.1071/IS18073
Submitted: 30 August 2018 Accepted: 21 January 2019 Published: 1 August 2019
Abstract
The first molecular phylogeny of Lynceus (Crustacea: Branchiopoda: Laevicaudata) is presented together with a description of a new species of laevicaudatan branchiopod from Chile, Lynceus huentelauquensis, sp. nov. DNA sequences were obtained from six species of Lynceus using freshly collected specimens from Europe, North America, South America, and Australia and combined with GenBank sequences from previous studies. Specimens of the new species were collected from a pool on the Huentelauquén Plains near Huentelauquén City. Our molecular analyses placed L. huentelauquensis, sp. nov. within Lynceus and close to a cluster of Australian species, and revealed morphological misidentifications, cross-contamination, or incorrect upload in earlier GenBank sequences. L. huentelauquensis, sp. nov. is separated from other Lynceus primarily by the morphology of the rostrum and the male claspers. L. huentelauquensis, sp. nov. is the first described laevicaudatan from Chile, the sixth from South America, and the 13th from the Americas. The morphology of laevicaudatans from the Americas is reviewed and an updated key to the (male) Lynceidae of the region is provided. Our study highlights the necessity of a revision of Laevicaudata using multiple genetic markers as well as thorough morphological studies on a greater number of taxa.
urn:lsid:zoobank.org:pub:9A783D96-B270-40DF-8361-11BA063C9A0F
Additional keywords: clam shrimp, Huentelauquén Plains, large Branchiopoda, 16S rDNA
References
Alvarez, M., San Martín, J., and Deil, U. (2013). Nanism and ephemerism as reasons for a hidden abundance in vernal pool plants: the example of Lepuropetalon spathulatum in Chile. Feddes Repertorium 123, 55–66.| Nanism and ephemerism as reasons for a hidden abundance in vernal pool plants: the example of Lepuropetalon spathulatum in Chile.Crossref | GoogleScholarGoogle Scholar |
Brady, G. S. (1886). Notes on freshwater Entomostraca from South Australia. Proceedings of the Scientific Meeting of the Zoological Society of London 1886, 82–93.
Brendonck, L., Rogers, D. C., Olesen, J., Weeks, S., and Hoeh, W. R. (2008). Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater. Hydrobiologia 595, 167–176.
| Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater.Crossref | GoogleScholarGoogle Scholar |
Crespo, F. A. (1996). A new record of the family Lynceidae Stebbing, 1902 (Branchiopoda, Conchostraca) from Argentina. Physis (Buenos Aires) 51, 21–22.
Daday, E. V. (1902). Mikroskopische Süsswasserthiere aus Patagonien, gesammelt von Dr. Filippo Sylvestri im Jahre 1899 und 1900. Természetrajzi Füzetek 25, 201–310.
Daday, E. (1927). Monographie systématique des Phyllopodes Conchostracés. Troisième partie (fin). Annales des Sciences Naturelles, Zoologie 10, 587–698.
de Los Ríos, P., Pizarro-Araya, J., Alfaro, F. M., and Zuleta, C. (2019). First descriptions of aquatic crustaceans in coastal plains in northern Chile (Huentelauquen, 31°S, Coquimbo region, Chile). Crustaceana 92, 73–81.
| First descriptions of aquatic crustaceans in coastal plains in northern Chile (Huentelauquen, 31°S, Coquimbo region, Chile).Crossref | GoogleScholarGoogle Scholar |
deWaard, J. R., Sacherova, V., Cristescu, M. E. A., Remigio, E. A., Crease, T. J., and Hebert, P. D. N. (2006). Probing the relationships of the branchiopod crustaceans. Molecular Phylogenetics and Evolution 39, 491–502.
| Probing the relationships of the branchiopod crustaceans.Crossref | GoogleScholarGoogle Scholar | 16406819PubMed |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |
Espejo, L., Kretschmer, N., Oyarzún, J., Meza, F., Núñez, J., Maturana, H., Soto, G., Oyarzo, P., Garrido, M., Suckel, F., Amezaga, J., and Oyarzún, R. (2012). Application of water quality indices and analysis of the surface water quality monitoring network in semiarid north-central Chile. Environmental Monitoring and Assessment 184, 5571–5588.
| Application of water quality indices and analysis of the surface water quality monitoring network in semiarid north-central Chile.Crossref | GoogleScholarGoogle Scholar | 21938385PubMed |
Fan, Y. P., Lu, B., and Yang, J. S. (2016). The complete mitogenome of the fairy shrimp Phallocryptus tserensodnomi (Crustacea: Anostraca: Thamnocephalidae). Mitochondrial DNA 27, 3113–3114.
| The complete mitogenome of the fairy shrimp Phallocryptus tserensodnomi (Crustacea: Anostraca: Thamnocephalidae).Crossref | GoogleScholarGoogle Scholar | 25707412PubMed |
Gajardo, R. (1994). ‘La Vegetación Natural de Chile: Clasificación y Distribución Geográfica.’ Editorial Universitaria, Santiago de Chile, Chile
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Kaisila, J., Haahtela, I., and Valtonen, T. (1963). The first record of Lynceus brachyurus O. F. Müller (Crustacea, Branchiopoda) in Finland. Aquilo, Series Zoologica 1, 17–23.
Kaji, T., Fritsch, M., Schwentner, M., Olesen, J., and Richter, S. (2014). Male claspers in clam shrimps (Crustacea, Branchiopoda) in the light of evolution: a case study on homology versus analogy. The Journal of Experimental Zoology B: Molecular and Developmental Evolution 322B, 269–280.
| Male claspers in clam shrimps (Crustacea, Branchiopoda) in the light of evolution: a case study on homology versus analogy.Crossref | GoogleScholarGoogle Scholar |
Koenemann, S., Jenner, R. A., Hoenemann, M., Stemme, T., and von Reumont, B. M. (2010). Arthropod phylogeny revisited, with a focus on crustacean relationships. Arthropod Structure & Development 39, 88–110.
| Arthropod phylogeny revisited, with a focus on crustacean relationships.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Liu, X. C., Li, H. W., Jermnak, U., and Yang, J. S. (2016). The complete mitogenome of the freshwater fairy shrimp Streptocephalus sirindhornae (Crustacea: Anostraca: Streptocephalidae). Mitochondrial DNA 27, 3189–3191.
| The complete mitogenome of the freshwater fairy shrimp Streptocephalus sirindhornae (Crustacea: Anostraca: Streptocephalidae).Crossref | GoogleScholarGoogle Scholar | 25693703PubMed |
Luebert, F., and Pliscoff, P. (2006). ‘Sinopsis Bioclimatica y Vegetacional de Chile.’ (Editorial Universitaria: Santiago.)
Maeda-Martínez, A. M., Obregón-Barboza, H., and García-Velazco, H. (2002). Branchiopoda: Cyclestherida, Laevicaudata, and Spinicaudata. In ‘Biodiversidad, Taxonomía y Biogeografía de Artrópodos de Mexico: Hacia una Síntesis de su Conocimiento. Volume III’. (Eds J. Llorente Bousquets, and J. J. Morrone.) pp. 223–331. (Universidad Nacional Autónoma de México: Mexico.)
Mantovani, B., Cesari, M., and Scanabissi, F. (2009). Molecular taxonomy and phylogeny of Italian Lepidurus taxa (Branchiopoda: Notostraca). The Italian Journal of Zoology 76, 358–365.
| Molecular taxonomy and phylogeny of Italian Lepidurus taxa (Branchiopoda: Notostraca).Crossref | GoogleScholarGoogle Scholar |
Martin, J. W., and Belk, D. (1988). Review of the clam shrimp family Lynceidae Stebbing, 1902 (Branchiopoda: Conchostraca) in the Americas. Journal of Crustacean Biology 8, 451–482.
| Review of the clam shrimp family Lynceidae Stebbing, 1902 (Branchiopoda: Conchostraca) in the Americas.Crossref | GoogleScholarGoogle Scholar |
Martin, J. W., Felgenhauer, B. E., and Abele, L. G. (1986). Redescription of the clam shrimp Lynceus gracilicornis (Packard) (Branchiopoda, Conchostraca, Lynceidae) from Florida, with notes on its biology. Zoologica Scripta 15, 221–232.
| Redescription of the clam shrimp Lynceus gracilicornis (Packard) (Branchiopoda, Conchostraca, Lynceidae) from Florida, with notes on its biology.Crossref | GoogleScholarGoogle Scholar |
Mathers, T. C., Hammond, R. L., Jenner, R. A., Zierold, T., Hänfling, B., and Gómez, A. (2013). High lability of sexual system over 250 million years of evolution in morphologically conservative tadpole shrimps. BMC Evolutionary Biology 13, .
| High lability of sexual system over 250 million years of evolution in morphologically conservative tadpole shrimps.Crossref | GoogleScholarGoogle Scholar | 23384124PubMed |
Olesen, J. (1998). A phylogenetic analysis of the Conchostraca and Cladocera (Crustacea, Branchiopoda, Diplostraca). Zoological Journal of the Linnean Society 122, 491–536.
| A phylogenetic analysis of the Conchostraca and Cladocera (Crustacea, Branchiopoda, Diplostraca).Crossref | GoogleScholarGoogle Scholar |
Olesen, J. (2009). Phylogeny of Branchiopoda (Crustacea) – character evolution and contribution of uniquely preserved fossils. Arthropod Systematics & Phylogeny 67, 3–39.
Olesen, J., Pöllabauer, C., Sigvardt, Z. M. S., and Rogers, D. C. (2016). A new species of Lynceus Müller, 1776 from New Caledonia (Crustacea: Branchiopoda: Laevicaudata) from dolines, with remarks on zoogeography. European Journal of Taxonomy 224, 1–18.
| A new species of Lynceus Müller, 1776 from New Caledonia (Crustacea: Branchiopoda: Laevicaudata) from dolines, with remarks on zoogeography.Crossref | GoogleScholarGoogle Scholar |
Palero, F., Guerao, G., Clark, P. F., and Abelló, P. (2009). The true identities of the slipper lobsters Nisto laevis and Nisto asper (Crustacea: Decapoda: Scyllaridae) verified by DNA analysis. Invertebrate Systematics 23, 77–85.
| The true identities of the slipper lobsters Nisto laevis and Nisto asper (Crustacea: Decapoda: Scyllaridae) verified by DNA analysis.Crossref | GoogleScholarGoogle Scholar |
Pessacq, P., Epele, L. B., and Rogers, D. C. (2011). A new species of Lynceus (Crustacea: Branchiopoda: Laevicaudata) from Patagonia, with comments on laevicaudatan systematics. Zootaxa 3043, 25–32.
Richter, S., Olesen, J., and Wheeler, W. C. (2007). Phylogeny of Branchiopoda (Crustacea) based on a combined analysis of morphological data and six molecular loci. Cladistics 23, 301–336.
| Phylogeny of Branchiopoda (Crustacea) based on a combined analysis of morphological data and six molecular loci.Crossref | GoogleScholarGoogle Scholar |
Roessler, E. W. (1995a). Review of Colombian Conchostraca (Crustacea) – ecological aspects and life cycles – families Lynceidae, Limnadiidae, Leptestheriidae and Metalimnadiidae. Hydrobiologia 298, 125–132.
| Review of Colombian Conchostraca (Crustacea) – ecological aspects and life cycles – families Lynceidae, Limnadiidae, Leptestheriidae and Metalimnadiidae.Crossref | GoogleScholarGoogle Scholar |
Roessler, E. W. (1995b). Review of Colombian Conchostraca (Crustacea) – morphotaxonomic aspects. Hydrobiologia 298, 253–262.
| Review of Colombian Conchostraca (Crustacea) – morphotaxonomic aspects.Crossref | GoogleScholarGoogle Scholar |
Rogers, D. C., and Olesen, J. (2016). Laevicaudata catalogus (Crustacea: Branchiopoda): an overview of diversity and terminology. Arthropod Systematics & Phylogeny 74, 221–240.
Rogers, D. C., and Padhye, S. (2015). Review of the large branchiopod crustacean fauna of the Indian subcontinent (Anostraca, Notostraca, Laevicaudata, Spinicaudata, Cyclestherida). Journal of Crustacean Biology 35, 392–406.
| Review of the large branchiopod crustacean fauna of the Indian subcontinent (Anostraca, Notostraca, Laevicaudata, Spinicaudata, Cyclestherida).Crossref | GoogleScholarGoogle Scholar |
Rogers, D. C., Olesen, J., and Martin, J. W. (2015). A new possibly parthenogenic species of Lynceus from Canada (Crustacea: Branchiopoda: Laevicaudata), with key to the Nearctic female Laevicaudata. Natural History Museum The University of Kansas 47, 1–9.
Schwentner, M., Timms, B. V., Bastrop, R., and Richter, S. (2009). Phylogeny of Spinicaudata (Branchiopoda, Crustacea) based on three molecular markers – an Australian origin for Limnadopsis. Molecular Phylogenetics and Evolution 53, 716–725.
| Phylogeny of Spinicaudata (Branchiopoda, Crustacea) based on three molecular markers – an Australian origin for Limnadopsis.Crossref | GoogleScholarGoogle Scholar | 19643195PubMed |
Schwentner, M., Richter, S., Rogers, D. C., and Giribet, G. (2018). Tetraconatan phylogeny with special focus on Malacostraca and Branchiopoda: highlighting the strength of taxon-specific matrices in phylogenomics. Proceedings. Biological Sciences 285, 20181524.
| Tetraconatan phylogeny with special focus on Malacostraca and Branchiopoda: highlighting the strength of taxon-specific matrices in phylogenomics.Crossref | GoogleScholarGoogle Scholar | 30135168PubMed |
Sigvardt, Z. M. S., and Olesen, J. (2014). Mating behaviour in laevicaudatan clam shrimp (Crustacea, Branchiopoda) and functional morphology of male claspers in a phylogenetic context: a video-based analysis. PLoS One 9, e84021.
| Mating behaviour in laevicaudatan clam shrimp (Crustacea, Branchiopoda) and functional morphology of male claspers in a phylogenetic context: a video-based analysis.Crossref | GoogleScholarGoogle Scholar |
Stenderup, J. T., Olesen, J., and Glenner, H. (2006). Molecular phylogeny of the Branchiopoda (Crustacea) – multiple approaches suggest a ‘diplostracan’ ancestry of the Notostraca. Molecular Phylogenetics and Evolution 41, 182–194.
| Molecular phylogeny of the Branchiopoda (Crustacea) – multiple approaches suggest a ‘diplostracan’ ancestry of the Notostraca.Crossref | GoogleScholarGoogle Scholar | 16904916PubMed |
Straškraba, M. (1965). Taxonomical studies on Czechoslovac Conchostraca II. Families Lynceidae and Cyzicidae. Vestnik Ceskoslovenske Spolecnosti Zoologicke Acta Societatis Zoologicae Bohemoslovenicae 29, 205–214.
Timms, B. V. (2013). A revision of the Australian species of Lynceus Müller, 1776 (Crustacea: Branchiopoda: Laevicaudata, Lynceidae). Zootaxa 3702, 501–533.
| A revision of the Australian species of Lynceus Müller, 1776 (Crustacea: Branchiopoda: Laevicaudata, Lynceidae).Crossref | GoogleScholarGoogle Scholar | 26146743PubMed |
von Reumont, B. M., Jenner, R. A., Wills, M. A., Dell’Ampio, E., Pass, G., Ebersberger, I., Meyer, B., Koenemann, S., Iliffe, T. M., Stamatakis, A., Niehuis, O., Meusemann, K., and Misof, B. (2012). Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Molecular Biology and Evolution 29, 1031–1045.
| Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda.Crossref | GoogleScholarGoogle Scholar | 22049065PubMed |
Zofkova, M. (2006). Evolutionary dynamics in ephemeral pools: inferences from genetic architecture of large branchiopods. Ph.D. Thesis. The University of Western Australia, Perth.
Zuleta, C., and Piñones, C. (2015). ‘Secano costero de Huentelauquén: Paisajes y Presencia Humana.’ (Ediciones Universidad de La Serena-Ministerio del Medio Ambiente : La Serena, Chile.)
Zuleta, C., Cea, A., Bravo, V., Castillo, R., Robles, M., Pizarro-Araya, J., Alfaro, F. M., De los Ríos-Escalante, P., and Piñones, C. (2019). Charcas Temporales de Huentelauquén (Canela, Región de Coquimbo). In ‘Humedales Costeros de la Región de Coquimbo: Biodiversidad, Vulnerabilidades & Conservación’. (Eds C. Zuleta and M. Contreras-López.) in press. (Ediciones Universidad de la Serena, La Serena, Chile.)