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A SYSTEMATIC STUDY of the GENUS EULIMNADIA Sadie K. Reed, R. Joel Duff, and Stephen C. Weeks

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A SYSTEMATIC STUDY of the GENUS EULIMNADIA Sadie K. Reed, R. Joel Duff, and Stephen C. Weeks JOURNAL OF CRUSTACEAN BIOLOGY, 35(3), 379-391, 2015 A SYSTEMATIC STUDY OF THE GENUS EULIMNADIA Sadie K. Reed, R. Joel Duff, and Stephen C. Weeks ∗ Program in Integrated Biosciences, Department of Biology, The University of Akron, Akron, OH 44325-3908, USA ABSTRACT The clam shrimp genus Eulimnadia Packard, 1874 is the most speciose and widely distributed in the Spinicaudata. Taxonomic determinations based on morphology have been controversial because of intraspecific variability in many of the characters used to date. Most recently, egg shell morphology has been the preferred source of species specific characters. We explore the phylogenetic relationships of 19 Eulimnadia species and assess previously proposed synonymies of E. diversa based on egg shell morphology. Phylogenetic studies were based on cytochrome b and elongation factor 1α, and were analyzed using Maximum Likelihood and Bayesian Inference approaches. Phylogenetic analyses support the monophyly of Eulimnadia, yet a large amount of polyphyly exists for species identified via morphology. Specimens of Eulimnadia diversa s.l. were highly unresolved and polyphyletic. Overall, species level phylogenetic resolution was low, emphasizing the great need for a systematic revision of Eulimnadia. KEY WORDS: Androdioecy, clam shrimp, hermaphrodites, Spinicaudata DOI: 10.1163/1937240X-00002345 INTRODUCTION presented a discussion of limnadiid generic relationships based on morphological characters. She chose to recognize the similarities of Eulimnadia and Limnadia by including Eulimnadia Packard, 1874 is classified within Limnadi- them in the subfamily Limnadiinae Burmeister, 1843. This idae along with Limnadia Brongniart, 1820, Limnadopsis taxonomic classification was based on a comparison of 10 Spencer and Hall, 1896, Imnadia Hertzog, 1935, Metalim- morphological characters (Straškraba, 1964). Rogers et al. nadia Mattox, 1952, Paralimnadia Sars, 1896, Afrolimnadia (2012) revised the extant genera of Limnadiidae based on Rogers et al., 2012, Calalimnadia Rogers et al., 2012, and the molecular analyses of Weeks et al. (2009) and provided Austrolimnadia Timms and Schwentner, 2012. Of these Eu- morphological characters specific to each genus. Yet species limnadia is the most speciose and widely distributed (Brtek, distinctions are still in need of study. 1997). The next most speciose genus is Limnadopsis, which Most molecular phylogenies to date have focused on contains 12 species (Schwentner et al., 2012). Brtek (1997) higher level analyses of the branchiopod families (Hanner compiled a checklist of the valid and invalid species names and Fugate, 1997; Spears and Abele, 2000; Braband et al., 2002). Braband et al. (2002) did a combined analysis of of the large Branchiopods, within which he listed 52 de- 12S rDNA and elongation factor 1α (EF1α) and found sup- scribed species of Eulimnadia, but only recognized 43 valid port for a sister relationship between (Imnadia and Limna- species (Table 1). Additionally, Brtek (1997) did not men- dia) and (Eulimnadia and Limnadopsis) that were both sup- tion three species that had been described prior to his check- ported as monophyletic clades. Hoeh et al. (2006), using list (Martin and Belk, 1988; Roessler, 1990), and since his 28S rDNA, 12S rDNA, and cytochrome b (cytb) sequences, list, an additional seven species have been described (Pereira found support for the monophyly of Eulimnadia but the sis- and Garcia, 2001; Durga-Prasad and Simhachalam, 2004; ter group remained ambiguous. However, Limnadopsis was Timms and McLay, 2005; Babu and Nandan, 2010; Rogers never found to be sister to Eulimnadia. Schwentner et al. et al., 2010) yielding a total of 53 species (Table 1). (2009) analyzed 41 species, including 15 of Eulimnadia, Webb and Bell (1979) synonymized Eulimnadia with with data from three genes: 28S, 16S, and cytochrome c oxidase I (COI). This study reached the same conclusions Limnadia, stating that within Spinicaudata, genus diagnos- as Hoeh et al. (2006) regarding the monophyly of Eulim- tic characters can be highly variable in different stages of nadia and lack of sister relationship with Limnadia.Inthe ontogeny, in different sexes, and in different species within same year, Weeks et al. (2009) reported strong support for the same genus. Martin and Belk (1988) and Belk (1989) the monophyly of Limnadiidae including the genera Eulim- disputed this reasoning, suggesting it was based on a sur- nadia, Metalimnadia, Imnadia, and Limnadopsis. Two unde- vey of poor taxonomic drawings in the literature, but never- scribed eulimnadoid species included in the analysis fall into theless recognized the morphological similarities of the ge- distinct clades, the first from the island Republic of Mauri- nera and assumed them to be sister taxa. In 1964 Straškraba tius and the second from South Africa. These two new taxa ∗ Corresponding author; e-mail: [email protected] © The Crustacean Society, 2015. Published by Brill NV, Leiden DOI:10.1163/1937240X-00002345 380 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 35, NO. 3, 2015 Table 1. (Continued.) Table 1. List of valid Eulimnadia species names along with generalized locality information obtained from the literature or from our own collec- Species Locality tions. Synonymies are indented underneath the valid taxon. Eulimnadia ovilunata Argentina Species Locality Martin and Belk, 1989 Eulimnadia ovisimilis Paraguay Eulimnadia acutirostris Daday, 1913 West Africa Martin and Belk, 1988 Eulimnadia aethiopica Daday, 1913 Sudan Eulimnadia packardiana Ishikawa, 1895 Japan Eulimnadia agassizii Packard, 1874 Massachusetts, Eulimnadia pulchra Mohammad, 1986 Iraq USA Eulimnadia similis Sars, 1900 India Eulimnadia stoningtonensis Berry, 1926 Eulimnadia subtropica Daday, 1913 Madagascar Eulimnadia alluaudi Daday, 1913 Madagascar Eulimnadia taoluoensis Hu, 1986 China Eulimnadia antillarum (Baird, 1852) Mexico, West Eulimnadia texana Packard, 1871 USA, Mexico Indies, Brazil Eulimnadia tropica Rammner, 1933 Caribbean Eulimnadia antlei Mackin, 1940 USA Islands Eulimnadia astraova BeIk, 1989 USA Eulimnadia azerbaidshanica Azerbaijan Smirnov, 1936 Eulimnadia azisi Babu and Nandan, 2010 India Eulimnadia behningi Smirnov, 1949 Uzbekistan were assigned by Rogers et al. (2012) the two generic names Eulimnadia belki Martin, 1989 Mexico, Calalimnadia and Afrolimnadia, respectively. Venezuela Rogers et al. (2012) resurrected the genus Paralimnadia Eulimnadia brasiliensis Sars, 1902 Brazil Sars, 1896 to encompass the Australian representatives of Eulimnadia braueriana Ishikawa, 1895 Japan Limnadia. They further noted the monophyly of (Eulimna- Eulimnadia chacoensis Gurney, 1931 Paraguay dia + Metalimnadia) and (Paralimnadia + Limnadopsis). Eulimnadia colombiensis Roessler, 1990 Colombia Weeks et al. (2009) analyzed a total of 71 specimens repre- Eulimnadia compressa (Baird, 1860) India senting 15 species of Eulimnadia. The analysis of multiple Eulimnadia chaperi (Simon, 1886) Eulimnadia curvirostris Roen, 1952 China specimens per species highlighted problematic species de- Eulimnadia cylindrova Belk, 1989 USA, Mexico, terminations for specimens of E. diversa, E. follisimilis, and Galapagos E. cylindrova which were not monophyletic in the phyloge- Eulimnadia dahli Sars, 1896 Australia netic analyses (Weeks et al., 2009). Eulimnadia diversa Mattox, 1937 USA While Brtek (1997) did recognize 43 valid species of Eulimnadia alineata Mattox, 1953 Eulimnadia (disregarding the inclusion in Limnadia), he also Eulimnadia francesae Mattox, 1953 suggested that many of these would be synonymized in the Eulimnadia inflecta Mattox, 1939 future, after careful examination of additional material. This Eulimnadia oryzae Mattox, 1954 Eulimnadia thompsoni Mattox, 1939 underscores the taxonomic difficulties that have faced this Eulimnadia ventricosa Mattox, 1953 group. Many of the early species descriptions were based on Eulimnadia dubia Daday, 1913 New Guinea few specimens, often from one locality. Frequently details Eulimnadia feriensis Dakin, 1914 Australia of characters were vague or missing and drawings have Eulimnadia follisimilis Venezuela been misleading (Belk, 1989). An excellent example of these Pereira and Garcia, 2001 issues is that of E. diversa. Mattox (1954) recognized 12 Eulimnadia garretti (Richters, 1882) Tahiti North American species of Eulimnadia. He found these to be Eulimnadia geayi Daday, 1913 Venezuela, distinct through the use of several morphological characters Colombia, Mexico including: carapace growth lines, carapace size and shape, Eulimnadia gibba Sars, 1900 India telson spines, head shape, male claspers, and antennae length Eulimnadia graniticola Rogers et al., 2010 Georgia, USA (Belk, 1989). However, Belk (1989) cites these characters as Eulimnadia gunturensis India unreliable due to high levels of intraspecific variability. He Radhakrishna and Durga-Prasad, 1976 also found that in some cases, such as that of E. alineata, Eulimnadia indocylindrova India the type specimens were immature. Like many since, he Durga-Prasad and Simhachalam, 2004 found egg morphology to be the most important in species Eulimnadia kobai Ueno, 1940 China diagnoses and subsequently synonymized six (E. inflecta, E. Eulimnadia magdalensis Roessler, 1990 Colombia thompsoni, E. ventricosa, E. francesae, E. oryzae, and E. Eulimnadia margaretae Bond, 1934 South Arabica Eulimnadia marplesi New Zealand alineata) of the North American species into E. diversa due Timms and McLay, 2005 to similarities in egg structure. However, while Belk (1989) Eulimnadia mauritiana (Guérin,
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