Analysing morphological variation of appendages and labrum in 10 species of Heterocypris Claus, 1893 (Podocopida : Cyprididae) with additional description of Heterocypris exigua
Tamara Karan-Žnidaršič A C , Vukica Vujić A and Ángel Baltanás BA Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia.
B Department of Ecology, Faculty of Sciences, Universidad Autónomade Madrid (UAM), 28049 Madrid, Spain.
C Corresponding author. Email: ktamara@bio.bg.ac.rs
Invertebrate Systematics 32(6) 1448-1464 https://doi.org/10.1071/IS18031
Submitted: 6 April 2018 Accepted: 9 July 2018 Published: 14 December 2018
Abstract
Natural selection can lead to speciation, but its effects depend on amount of morphological variation within populations. In Ostracoda, the appendages enclosed within the calcified carapace are less influenced by environmental conditions in comparison with carapace valves. Here, we explored morphological variation of appendages and labrum in cosmopolitan genus Heterocypris, investigating the species occurring in Europe. With the aim to overcome taxonomical problems, both traditional and geometric morphometrics were applied. The relative lengths were analysed by one-way ANOVA and post-hoc tests to determine interspecific variation and sexual dimorphism. Significant traits were further analysed by Canonical Variate Analysis separately for males and females as segment width/length ratios and relative length of claws and setae ratios. Landmark-based geometric morphometrics were applied to analyse shape variation of the labrum and traits of the maxillular palp. From this, a new perspective on morphological variation within this genus emerged. Relative measurements of the second segment of the maxillular palp, and relative lengths of the natatory setae were found to be the characters that contribute most to discrimination among Heterocypris species. The most important discriminant traits in females are the relative lengths of the G2 and G1 claws. Heterocypris exigua is additionally described, as all findings demonstrated that this is the most distinctive species, the most similar to H. gevgelica. In conclusion, we found that in comparison with maxillular palp and other analysed characters, labrum traits showed as more reliable and deserve more attention in descriptions of new species.
Additional keywords: comparative morphology, morphometrics, taxonomy.
References
Abe, K., Reyment, R. A., Bookstein, F. L., Honigstein, A., Almogi-Labin, A., Rosenfeld, A., and Hermelin, O. (1988). Microevolution in two species of ostracods from the Santonian (Cretaceous) of Israel. Historical Biology 1, 303–322.| Microevolution in two species of ostracods from the Santonian (Cretaceous) of Israel.Crossref | GoogleScholarGoogle Scholar |
Aguilar-Alberola, J. A., and Mesquita-Joanes, F. (2013). Ontogeny of Heterocypris bosniaca (Ostracoda: Cyprididae): description of postembryonic instars and rediscovery of the neglected A-9 stage. Journal of Crustacean Biology 33, 348–371.
| Ontogeny of Heterocypris bosniaca (Ostracoda: Cyprididae): description of postembryonic instars and rediscovery of the neglected A-9 stage.Crossref | GoogleScholarGoogle Scholar |
Alves, V. M., Moura, M. O., and de Carvalho, C. J. B. (2016). Wing shape is influenced by environmental variability in Polietina orbitalis (Stein) (Diptera: Muscidae). Revista Brasileira de Entomologia 60, 150–156.
| Wing shape is influenced by environmental variability in Polietina orbitalis (Stein) (Diptera: Muscidae).Crossref | GoogleScholarGoogle Scholar |
Baltanás, Á. (2008). Geometric morphometrics: a contribution to the study of shape variability in Ostracods. In ‘Contribution to the Geometric Morphometrics’. (Eds D. L. Danielopol, M. Gross and W. E. Piller.) pp. 3–15. (Berichte des Institutes für Erdwissenschaften, Karl-Franzens Universität Graz: Graz, Austria.)
Baltanás, Á., and Danielopol, D. L. (2011). Geometric morphometrics and its use in ostracod research: a short guide. Joannea-Geologie und Palaontologie 11, 235–272.
Baltanás, A., and Geiger, W. (1998). Intraspecific morphological variability: morphometry of valve outlines. In ‘Sex and Parthenogenesis’. (Ed. K. Martens.) pp. 127–142. (Backhuys Publishers, Leiden, The Netherlands)
Broodbakker, N. W. (1982). The genus Heterocypris (Crustacea, Ostracoda) in the West Indies. Part II. Carapace length, ecology and zoogeography. Bijdragen tot de Dierkunde 53, 115–134.
Broodbakker, N. W. (1983). The genus Hemicypris (Crustacea, Ostracoda) in the West Indies. Bijdragen tot de Dierkunde 53, 135–157.
Cooper, W. J., Albertson, R. C., Jacob, R. E., and Westneat, M. W. (2014). Re-description and reassignment of the damselfish Abudefduf luridus (Cuvier, 1830) using both traditional and geometric morphometric approaches. Copeia 2014, 473–480.
| Re-description and reassignment of the damselfish Abudefduf luridus (Cuvier, 1830) using both traditional and geometric morphometric approaches.Crossref | GoogleScholarGoogle Scholar |
Darwin, C. (1871). ‘The Descent of Man and Selection in Relation to Sex (Reprinted in 1959).’ (Modern Library: New York, NY, USA.)
Deb, M. (1983). Brief descriptions of new species of Ostracoda: Crustacea from Maharashtra State (India). Records of the Zoological Survey of India 81, 135–166.
| Brief descriptions of new species of Ostracoda: Crustacea from Maharashtra State (India).Crossref | GoogleScholarGoogle Scholar |
Drake, A. G., and Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: disparity and modularity. American Naturalist 175, 289–301.
| Large-scale diversification of skull shape in domestic dogs: disparity and modularity.Crossref | GoogleScholarGoogle Scholar |
Eberhard, W. G., Huber, B. A., Briceño, R. D., Salas, I., and Rodriguez, V. (1998). One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52, 415–431.
| One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders.Crossref | GoogleScholarGoogle Scholar |
Gauthier, H., and Brehm, V. (1928). Ostracodes et cladocères de l’Algérie et de la Tunisie. Troisième note. Bulletin De La Société D’Histoire Naturelle De L’Afrique du Nord 19, 114–121.
Gidaszewski, N. A., Baylac, M., and Klingenberg, C. P. (2009). Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evolutionary Biology 9, 110.
| Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup.Crossref | GoogleScholarGoogle Scholar |
Gras, R., Golestani, A., Hendry, A. P., and Cristescu, M. E. (2015). Speciation without pre-defined fitness functions. PLoS One 10, e0137838.
| Speciation without pre-defined fitness functions.Crossref | GoogleScholarGoogle Scholar |
Guillette, L. J., Pickford, D. B., Crain, D. A., Rooney, A. A., and Percival, H. F. (1996). Reduction in penis size and plasma testosterone concentrations in juvenile alligators living in a contaminated environment. General and Comparative Endocrinology 101, 32–42.
| Reduction in penis size and plasma testosterone concentrations in juvenile alligators living in a contaminated environment.Crossref | GoogleScholarGoogle Scholar |
Horne, D. J., Cohen, A., and Martens, K. (2002). Taxonomy, morphology and biology of Quaternary and living Ostracoda. The Ostracoda: Applications in Quaternary Research 131, 5–36.
Iepure, S., Namiotko, T., and Danielopol, D. L. (2007). Evolutionary and taxonomic aspects within the species group Pseudocandona eremita (Vejdovský) (Ostracoda, Candonidae). Hydrobiologia 585, 159–180.
| Evolutionary and taxonomic aspects within the species group Pseudocandona eremita (Vejdovský) (Ostracoda, Candonidae).Crossref | GoogleScholarGoogle Scholar |
Jojić, V., Nenadović, J., Blagojević, J., Paunović, M., Cvetković, D., and Vujošević, M. (2012). Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation. Zoologischer Anzeiger 251, 26–37.
| Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation.Crossref | GoogleScholarGoogle Scholar |
Karan-Žnidaršič, T., and Petrov, B. (2014). Morphological differentiation of seven species of the genus Heterocypris Claus, 1892 (Ostracoda, Crustacea) based on the upper lip. Zootaxa 3852, 321–335.
| Morphological differentiation of seven species of the genus Heterocypris Claus, 1892 (Ostracoda, Crustacea) based on the upper lip.Crossref | GoogleScholarGoogle Scholar |
Karanovic, I. (2012). ‘Recent Freshwater Ostracods of the World: Crustacea, Ostracoda, Podocopida.’ (Springer Science & Business Media, Springer-Verlag Berlin Heidelberg, Germany)
Karanovic, I., Tanaka, H., and Tsukagoshi, A. (2016). Congruence between male upper lip morphology and molecular phylogeny in Parapolycope (Ostracoda), with two new species from Korea. Invertebrate Systematics 30, 231–254.
| Congruence between male upper lip morphology and molecular phylogeny in Parapolycope (Ostracoda), with two new species from Korea.Crossref | GoogleScholarGoogle Scholar |
Karanovic, I., Lavtižar, V., and Djurakic, M. (2017). A complete survey of normal pores on a smooth shell ostracod (Crustacea): landmark-based versus outline geometric morphometrics. Journal of Morphology 278, 1091–1104.
| A complete survey of normal pores on a smooth shell ostracod (Crustacea): landmark-based versus outline geometric morphometrics.Crossref | GoogleScholarGoogle Scholar |
Kesling, R. V. (1951). The Morphology of Ostracod Molt Stages. In ‘Illinois Biological Monographs, Vol. 21, Series 1–3’. (University Illinois Press: Urbana-Champaign, IL, USA.)
Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.
| MorphoJ: an integrated software package for geometric morphometrics.Crossref | GoogleScholarGoogle Scholar |
Klingenberg, C. P. (2013). Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24, 15–24.
Klingenberg, C. P., and Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology 59, 245–261.
| Testing and quantifying phylogenetic signals and homoplasy in morphometric data.Crossref | GoogleScholarGoogle Scholar |
Koenders, A., Schön, I., Halse, S., and Martens, K. (2017). Valve shape is not linked to genetic species in the Eucypris virens (Ostracoda, Crustacea) species complex. Zoological Journal of the Linnean Society 180, 36–46.
Kong, Q., Karanovic, I., and Yu, N. (2014). Phylogeny of the genus Chrissia (Ostracoda: Cyprididae) with description of a new species from China. Journal of Crustacean Biology 34, 782–794.
| Phylogeny of the genus Chrissia (Ostracoda: Cyprididae) with description of a new species from China.Crossref | GoogleScholarGoogle Scholar |
Lazić, M. M., Carretero, M. A., Crnobrnja-Isailović, J., and Kaliontzopoulou, A. (2015). Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. American Naturalist 185, 44–58.
| Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape.Crossref | GoogleScholarGoogle Scholar |
Lee, M. S., and Palci, A. (2015). Morphological phylogenetics in the genomic age. Current Biology 25, R922–R929.
| Morphological phylogenetics in the genomic age.Crossref | GoogleScholarGoogle Scholar |
Maddocks, R. F. (1988). Multivariate analysis of leg morphology of Macrocyprididae. Developments in Palaeontology and Stratigraphy 11, 219–234.
| Multivariate analysis of leg morphology of Macrocyprididae.Crossref | GoogleScholarGoogle Scholar |
Martens, K. (1996). On Heterocypris reptans (Kaufmann, 1900) (Ostracoda) Cyprididae, a new record of Israel. Israel Journal of Zoology 42, 287–291.
Martens, K., and Savatenalinton, S. (2011). A subjective checklist of the recent, freeliving, non-marine Ostracoda (Crustacea). Zootaxa 2855, 1–79.
Martens, K., Rossetti, G., and Geiger, W. (1998). Intraspecific morphological variability of limbs. In ‘Sex and Parthenogenesis. Evolutionary Ecology of Reproductive Modes in Non-Marine Ostracods’. (Ed. K. Martens.) pp. 143–155. (Backhuys Publishers: Leiden, Netherlands.)
Martens, K., Schwartz, S. S., Meisch, C., and Blaunstein, L. (2002). Non-marine Ostracoda Crustacea) of Mount Carmel (Israel), with taxonomic notes on Eucypridinae and circum-Mediterranean Heterocypris. Israel Journal of Zoology 48, 53–70.
| Non-marine Ostracoda Crustacea) of Mount Carmel (Israel), with taxonomic notes on Eucypridinae and circum-Mediterranean Heterocypris.Crossref | GoogleScholarGoogle Scholar |
Martins, M. J. F., Hunt, G., Lockwood, R., Swaddle, J. P., and Horne, D. J. (2017). Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda). PLoS One 12, e0177791.
| Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda).Crossref | GoogleScholarGoogle Scholar |
Meisch, C. (2000). Freshwater Ostracoda of western and central Europe. In ‘Süßwasserfauna von Mitteleuropa 8(3)’. (Eds J. Schwoerbel and P. Zwick.) pp. 522. (Spektrum Akademischer Verlag: Heidelberg, Berlin.)
Miller, J. P. (2016). Geometric morphometric analysis of the shell of Cerion mumia (Pulmonata: Cerionidae) and related species. Folia Malacologica 24, 239–250.
| Geometric morphometric analysis of the shell of Cerion mumia (Pulmonata: Cerionidae) and related species.Crossref | GoogleScholarGoogle Scholar |
Møller, A. P., Sanotra, G. S., and Vestergaard, K. S. (1999). Developmental instability and light regime in chickens (Gallus gallus). Applied Animal Behaviour Science 62, 57–71.
| Developmental instability and light regime in chickens (Gallus gallus).Crossref | GoogleScholarGoogle Scholar |
Moshayedi, F., Eagderi, S., and Rabbaniha, M. (2017). Allometric growth pattern and morphological changes of green terror Andinoacara rivulatus (Günther, 1860) (Cichlidae) during early development: comparison of geometric morphometric and traditional methods. Iranian Journal of Fisheries Science 16, 222–237.
Namiotko, T., Danielopol, D., and Baltanás, Á. (2011). Soft body morphology, dissection and slide-preparation of Ostracoda: a primer. Joannea-Geologie und Palaontologie 11, 327–343.
Paris, T. M., Allan, S. A., Hall, D. G., Hentz, M. G., Croxton, S. D., Ainpudi, N., and Stansly, P. A. (2017). Effects of temperature, photoperiod, and rainfall on morphometric variation of Diaphorina citri (Hemiptera: Liviidae). Environmental Entomology 46, 143–158.
Perrard, A., Lopez-Osorio, F., and Carpenter, J. M. (2016). Phylogeny, landmark analysis and the use of wing venation to study the evolution of social wasp (Hymenoptera: Vespidae: Vespinae). Cladistics 32, 406–425.
| Phylogeny, landmark analysis and the use of wing venation to study the evolution of social wasp (Hymenoptera: Vespidae: Vespinae).Crossref | GoogleScholarGoogle Scholar |
Petkowski, T. K., and Keyser, D. (1995). Neue und seltene limnische Ostracoden aus Mazedonien, (Crustacea: Ostracoda, Podocopida). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 92, 295–314.
Petkowski, T. K., Scharf, B., and Keyser, D. (2000). New and little known ostracods of the genus Heterocypris (Crustacea, Ostracoda) from the Balkan Peninsula. Limnologica 30, 45–57.
| New and little known ostracods of the genus Heterocypris (Crustacea, Ostracoda) from the Balkan Peninsula.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2008). R version 3.5.1 (2018-07-02): a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at: http://www.R-project.org [Verified 26 November 2018]
Ramírez-Sánchez, M. M., De Luna, E., and Cramer, C. (2016). Geometric and traditional morphometrics for the assessment of character state identity: multivariate statistical analyses of character variation in the genus Arrenurus (Acari, Hydrachnidia, Arrenuridae). Zoological Journal of the Linnean Society 177, 720–749.
| Geometric and traditional morphometrics for the assessment of character state identity: multivariate statistical analyses of character variation in the genus Arrenurus (Acari, Hydrachnidia, Arrenuridae).Crossref | GoogleScholarGoogle Scholar |
Rasouli, H., Scharf, B., Meisch, C., and Aygen, C. (2016). An updated checklist of the recent non-marine Ostracoda (Crustacea) of Iran, with a redescription of Eucypris mareotica (Fischer, 1855). Zootaxa 4154, 273–292.
| An updated checklist of the recent non-marine Ostracoda (Crustacea) of Iran, with a redescription of Eucypris mareotica (Fischer, 1855).Crossref | GoogleScholarGoogle Scholar |
Rohlf, F. J. (2008). ‘TpsDig, Version 2.12.’ (SUNY at Stony Brook: Stony Brook, NY, USA.)
Sánchez-González, J. R., Baltanás, Á., and Danielopol, D. L. (2004). Patterns of morphospace occupation in recent Cypridoidea (Crustacea, Ostracoda). Revista Española de Micropaleontología 36, 13–27.
Santos, E., Gómez-Olivencia, A., Arlegi, M., and Arsuaga, J. L. (2017). Cranial morphological differences within U. deningeri–U. spelaeus lineage: a double traditional and geometric morphometrics approach. Quaternary International 433, 347–362.
| Cranial morphological differences within U. deningeri–U. spelaeus lineage: a double traditional and geometric morphometrics approach.Crossref | GoogleScholarGoogle Scholar |
Sheets, H. D. (2003). ‘IMP: Integrated Morphometrics Package.’ (Department of Physics, Canisius College: Buffalo, NY, USA.) Available online http://www3.canisius.edu/~sheets/morphsoft.html [Verified 25 November 2018]
Sherratt, E., Klingenberg, C. P., Wilkinson, M., and Gower, D. J. (2014). Evolution of cranial shape in caecilians (Amphibia: Gymnophiona). Evolutionary Biology 41, 528–545.
| Evolution of cranial shape in caecilians (Amphibia: Gymnophiona).Crossref | GoogleScholarGoogle Scholar |
Smith, R. J., and Matzke-Karasz, R. (2008). The organ on the first segment of the cypridoidean (Ostracoda, Crustacea) antennule: morphology and phylogenetic significance. Senckenbergiana lethaea 88, 127–140.
StatSoft, Inc. (1997). ‘Statistica.’(StatSoft: Tulsa, OK, USA.)
Sywula, T. (1968). Notes on Ostracoda. II. On some Bulgarian species. Bulletin de la Société des Amis des Sciences et des Lettres de Poznań Serie D 8, 11–42.
Urbanelli, S., Porretta, D., Mastrantonio, V., Bellini, R., Pieraccini, G., Romoli, R., Crasta, G., and Nascetti, G. (2014). Hybridization, natural selection, and evolution of reproductive isolation: a 25-years survey of an artificial sympatric area between two mosquito sibling species of the Aedes mariaecomplex. Evolution 68, 3030–3038.
| Hybridization, natural selection, and evolution of reproductive isolation: a 25-years survey of an artificial sympatric area between two mosquito sibling species of the Aedes mariaecomplex.Crossref | GoogleScholarGoogle Scholar |
Victor, R., and Fernando, C. H. (1980). On Heterocypris makua (Tressler) 1937, a freshwater ostracod (Crustacea: Ostracoda) from the Hawaiian Islands, with notes on the other species of the genus. Canadian Journal of Zoology 58, 1288–1297.
| On Heterocypris makua (Tressler) 1937, a freshwater ostracod (Crustacea: Ostracoda) from the Hawaiian Islands, with notes on the other species of the genus.Crossref | GoogleScholarGoogle Scholar |
Viehberg, F. A. (2002). A new and simple method for qualitative sampling of meiobenthoscommunities. Limnologica – Ecology and Management of Inland Waters 32, 350–351.