An Improved Taxonomic Sampling Is a Necessary but Not Sufficient Condition for Resolving Inter-Families Relationships in Caridean Decapods
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An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods L. Aznar-Cormano, J. Brisset, T.- Y. Chan, L. Corbari, N. Puillandre, J. Utge, M. Zbinden, D. Zuccon & S. Samadi Genetica An International Journal of Genetics and Evolution ISSN 0016-6707 Genetica DOI 10.1007/s10709-014-9807-0 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. This e- offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. 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Samadi Received: 17 May 2014 / Accepted: 10 December 2014 Ó Springer International Publishing Switzerland 2015 Abstract During the past decade, a large number of better phylogenetic resolution for the inter-families rela- multi-gene analyses aimed at resolving the phylogenetic tionships. The rich collections of the Muse´um National relationships within Decapoda. However relationships d’Histoire Naturelle de Paris are used for sampling as far as among families, and even among sub-families, remain possible at least two species of two different genera for poorly defined. Most analyses used an incomplete and each family or subfamily. All potential markers are tested opportunistic sampling of species, but also an incomplete over this sampling. For some coding genes the amplifica- and opportunistic gene selection among those available for tion success varies greatly among taxa and the phyloge- Decapoda. Here we test in the Caridea if improving the netic signal is highly saturated. This result probably taxonomic coverage following the hierarchical scheme of explains the taxon-heterogeneity among previously pub- the classification, as it is currently accepted, provides a lished studies. The analysis is thus restricted to the genes homogeneously amplified over the whole sampling. Thanks to the taxonomic sampling scheme the monophyly Electronic supplementary material The online version of this of most families is confirmed. However the genes com- article (doi:10.1007/s10709-014-9807-0) contains supplementary material, which is available to authorized users. monly used in Decapoda appear non-adapted for clarifying inter-families relationships, which remain poorly resolved. L. Aznar-Cormano Á L. Corbari Á N. Puillandre Á D. Zuccon Á Genome-wide analyses, like transcriptome-based exon & S. Samadi ( ) capture facilitated by the new generation sequencing ISYEB - UMR 7205 – CNRS, MNHN, UPMC, EPHE, Muse´um National d’Histoire Naturelle, De´partement Syste´matique et methods might provide a sounder approach to resolve deep Evolution, Sorbonne Universite´s, CP26, 57 rue Cuvier, and rapid radiations like the Caridea. 75231 Paris Cedex 05, France e-mail: [email protected] Keywords Caridea Á Phylogeny Á Museum specimens J. Brisset Direction des Collections, Muse´um National d’Histoire Naturelle, 57 rue Cuvier, 75005 Paris, France Introduction T.-Y. Chan Institute of Marine Biology and Centre of Excellence for the During the last decade, many efforts have been employed Oceans, National Taiwan Ocean University, Keelung, Taiwan to resolve, using multi-gene approaches, the deeper nodes in the phylogeny of Decapoda (e.g. Martin et al. 2010; J. Utge Á D. Zuccon Ahyong et al. 2011; Tsang et al. 2014). However, the Service de Syste´matique Mole´culaire, UMS2700 MNHN-CNRS, De´partement Syste´matique et Evolution, Muse´um National comparison among molecular studies gives a picture as d’Histoire Naturelle, 43 rue Cuvier, 75005 Paris, France contradictory as are the morphological studies. As pointed out for example by Shen et al. (2013) or Tsang et al. (2014) M. Zbinden unbalanced taxon sampling is a major source of incon- Biologie des Organismes Aquatiques et Ecosyste`mes, UMR7208, MNHN-CNRS-IRD-UPMC, Muse´um National gruence among multi-gene analyses. Moreover, most of the d’Histoire Naturelle, Paris, France available datasets differ both in taxon sampling and in gene 123 Author's personal copy Genetica sampling. As a consequence it is very difficult to combine the family level and to infer inter-familial relationships and compare the results among studies. The objective of using within each family as far as possible at least two this paper is to test if the incongruence comes primarily species from two distinct genera. from incomplete taxon and gene sampling or from a lack of phylogenetic signal in the genetic markers used in pub- lished datasets. For testing this hypothesis, we take ad- Materials and methods vantage of the large Decapoda collection of the Muse´um National d’Histoire Naturelle of Paris (MNHN) which The state-of-the-art of Caridean classification and taxon benefit from 40 years of marine expeditions as part of the selection ongoing Tropical Deep-Sea Benthos program, led by the MNHN and the Institut de Recherche pour le De´veloppe- Several classifications have been proposed for the Caridea. ment (IRD). This program has generated an important flow The classification used in WoRMS (World Register of of new material from the Pacific and Indian Oceans that Marine Species: www.marinespecies.org) is a synthesis of have been studied by an active network of taxonomists current proposals. This classification is primarily based on (Richer de Forges et al. 2013). This collection has also the classification proposed by De Grave et al. (2009) using been shown to be an adequate source of specimens for a comparative morphology approach. The Carideorum molecular analysis and was used in large DNA-barcoding Catalogus (De Grave and Fransen 2011) and recent projects (Puillandre et al. 2012; Zuccon et al. 2012). molecular phylogenies (Page et al. 2008b; Bracken et al. To perform such an analysis we selected the Caridea 2010; Chan et al. 2010; De Grave et al. 2010, 2014; Short that, with more than 3,200 extant species, is after the et al. 2013) provided five main modifications to the clas- Brachyura, the second most speciose infraorder of De- sification of De Grave et al. (2009). First, the Procarididae capoda (De Grave et al. 2009). Caridean shrimps are pre- were excluded from the Caridea and included in a distinct sent worldwide, from tropical to polar regions, both in infraorder, the Procarididea (Bracken et al. 2010). Second, marine and freshwater environments. If the definition of the Oplophoridae were shown to be polyphyletic (Chan Caridea is not questioned (e.g. De Grave et al. 2009; et al. 2010) and thus separated into two distinct families, Bracken et al. 2010; Shen et al. 2013), the classification at the Acanthephyridae and the Oplophoridae s.s.. These two the superfamily and family levels is far from being re- families were included in the same superfamily, the solved. Several studies use a molecular phylogenetic ap- Oplophoroidea. Third, two genera, Eugonatonotus and proach to discuss the classification. However, the results Galatheacaris, were synonymized and placed in the remain unsatisfactory because none of the studies com- Eugonatonotidae (De Grave et al. 2010). Fourth, the family bined a wide taxonomic coverage of Caridean diversity and Kakaducarididae was synonymized with Palaemonidae a phylogenetic signal in the sampled genetic markers that (Short et al. 2013). The fifth is a just published work (De provides support for the family-level relationships. For Grave et al. 2014) separating Hippolytidae into five example, the study of Bracken et al. (2009) includes 31 of families, namely Merguiidae, Bythocarididae, Thoridae, the 38 currently accepted families, with 17 families rep- Hippolytidae s.s. and Lysmatidae. In this revised classifi- resented by at least 2 species, but only 2 non-coding genes cation, 14 superfamilies and 38 families are considered as (mitochondrial 16S and nuclear 18S). Conversely, Li et al. valid (Table 1). Because the goal of the study was to test (2011) use 5 nuclear genes (18S and 4 coding genes: NaK, the monophyly of these families and the relationships PEPCK, H3 and enolase) but only 20 Caridean families among them, we tried to include in the sampling at least with only 10 of them represented by at least 2 species. The two genera, each represented by at least two species, for as aim of the present study is to provide a multi-gene analysis many families as possible. at the family-level based on an improved taxonomic sam- The MNHN collections were screened to select speci- pling of the Caridea. To enhance the genetic sampling we mens based on their taxonomic identification but also based also tested all the genetic markers used in the recent De- on the availability of field data (i.e. precise location, depth, capoda literature and explored the public genetic databases habitat, etc.). To increase the success of the DNA se- to identify potential new markers. The main sources of quencing, we also considered additional criteria such as the markers were the recent articles on Caridea (Bracken et al. sampling dates and the apparent conservation state of the 2009; Chan et al. 2010; Li et al. 2011; Kou et al. 2013) and specimen. Specimens that might have been previously Decapoda phylogeny (Toon et al.