The “Crustacean Seas” — an Evolutionary Perspective on the Ponto–Caspian Peracarids
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505 The “Crustacean Seas” — an evolutionary perspective on the Ponto–Caspian peracarids Melania E.A. Cristescu and Paul D.N. Hebert Abstract: A spectacular adaptive radiation of crustaceans has occurred in the Black, Caspian, and Aral seas. This study tests several evolutionary scenarios based on the extent of genetic differentiation and the phylogenetic relation- ships among endemic mysids and gammarid amphipods from the Black and Caspian seas. Molecular phylogenies for these taxa were based on two mitochondrial genes: cytochrome c oxidase subunit I and the large ribosomal RNA sub- unit (16S), and one nuclear gene, the large ribosomal RNA subunit (28S). The results support the monophyly of the Ponto–Caspian gammarids (genera Dikerogammarus, Echinogammarus, Obesogammarus, and Pontogammarus), suggest- ing their origin from one colonization event. By contrast, several colonization events preceded the radiation of the Ponto–Caspian mysids (genera Limnomysis and Paramysis). Levels of intraspecific divergence were variable, with mysids showing either no geographic structure or deep genetic splits reflecting a long history of reproductive isolation between populations in marine settings and those in fresh waters. These findings suggest that the diversity of the Ponto–Caspian crustaceans has been underestimated and that species regarded as euryhaline are often composed of dis- tinct evolutionary groups whose taxonomic status should be reevaluated. Résumé : Il s’est produit une extraordinaire radiation des crustacés dans la mer Noire, la mer Caspienne et la mer d’Aral. Nous évaluons plusieurs scénarios évolutifs basés sur l’étendue de la différentiation génétique et les relations phylogénétiques chez les mysidés et les amphipodes gammaridés endémiques des mers Noire et Caspienne. Les phylo- génies moléculaires de ces taxons se basent sur deux gènes mitochondriaux, la sous-unité I de la cytochrome c oxydase et la grande sous-unité d’ARN ribosomique (16S), ainsi qu’un gène nucléaire, la grande sous-unité d’ARN ribosomique (28S). Nos résultats appuient l’hypothèse de la monophylie des gammaridés Ponto–Caspiens (genres Dikerogammarus, Echinogammarus, Obesogammarus et Pontogammarus), ce qui laisse croire qu’ils sont issus d’un même épisode de colonisation. En revanche, plusieurs épisodes de colonisation ont précédé la radiation des mysidés Ponto–Caspiens (genres Limnomysis et Paramysis). Les niveaux de divergence interspécifique sont variables : chez les mysidés, ou bien il n’y a pas de structure géographique, ou alors il y a d’importantes divergences génétiques qui reflètent une longue période d’isolement génétique entre les populations des milieux marins et celles d’eau douce. Ces résultats indiquent que la diversité des crustacés ponto-caspiens a été sous-estimée et que les espèces considérées comme euryhalines sont souvent composées de groupes évolutifs distincts dont le statut taxonomique a besoin d’être réévalué. [Traduit par la Rédaction] Cristescu and Hebert 517 Introduction endemics are confined to the Caspian Sea, this region has been considered the center for their radiation (Zenkevitch Many groups of organisms including fishes, mollusks, tur- 1963). As a result of this diversity, the Caspian Sea has been bellarians, and crustaceans have radiated in the Ponto– nicknamed the “Crustacean Sea”. However, its sibling seas, Caspian biogeographic region, which includes the Black, the Black and Azov seas, also support a substantial number Azov, Caspian, and Aral seas. However, the endemism in of endemics in their less saline estuaries, peripheral lakes, varied crustacean lineages (e.g., cladocerans, copepods, and rivers. In fact, almost 50% of Ponto–Caspian taxa are cumaceans, decapods, amphipods, and mysids) is signifi- shared between these basins and their evolutionary origin is cantly higher than in most other animal groups. For exam- particularly ambiguous. ple, more than 70 endemic amphipods and approximately 28 The four basins in the Ponto–Caspian region formed some mysid species have been described from the Ponto–Caspian 6 million years (Mys) ago following disintegration of the region (C|r|uÕu 1943; B|cescu 1954; Barnard and Barnard Paratethys Sea, an arm of the more extensive Tethys Sea 1983). In fact, the Ponto–Capian mysid fauna is the most di- (Dumont 1998). The shared occurrence of species in the verse fresh–brackish water mysid fauna in the world Black and Caspian seas could be explained by either these (B|cescu 1954; Mauchline 1980). Since most of these late Miocene – early Pliocene vicariance events that sepa- Received 19 April 2004. Accepted 25 October 2004. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on 31 March 2005. J18075 M.E.A. Cristescu1,2 and P.D.N. Hebert. Department of Zoology, University of Guelph, Guelph, ON N1G 2W1, Canada. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN 47405, USA. Can. J. Fish. Aquat. Sci. 62: 505–517 (2005) doi: 10.1139/F04-210 © 2005 NRC Canada 506 Can. J. Fish. Aquat. Sci. Vol. 62, 2005 rated the basins or more recent (late Pleistocene) dispersal arose through the recurrent colonization of each basin. Simi- from the Caspian Sea into the Black Sea. This matter is un- larly, the timing of speciation events is poorly understood. resolved. Several authors have suggested that most Ponto– The present study examines the extent of genetic differen- Caspian lineages originated long before the present basin tiation and phylogenetic relationship among six species of configuration, possibly during the late Miocene (B|cescu mysids and eight species of gammarid amphipods from the 1940; Barnard and Barnard 1983; Dumont 2000), while oth- Black and Caspian seas. Additionally, taking these crusta- ers argued for a more recent Pliocene or Pleistocene origin ceans as an example, this study explores the tempo and the (Mordukhai-Boltovskoi 1964; Grigorovich et al. 2003). mode of speciation responsible for the high species richness The Ponto–Caspian mysids have been partitioned into nine in the Ponto–Caspian area. genera: Acanthomysis, Caspiomysis, Diamysis, Hemimysis, Katamysis, Limnomysis, Mysis, Paramysis, and Schistomysis Materials and methods (B|cescu 1940, 1954). Väinölä (1995) showed that the pe- lagic flock of Caspian Mysis (Mysis microphthalma, Mysis am- Taxon sampling blyops, and Mysis caspia) reflects a recent intralacustrine Fourteen Ponto–Caspian crustacean species, including six radiation, but their relationships with the other endemic mysid mysids and eight amphipods, were analyzed in this study genera have not been investigated. The present study ad- (Table 1). Samples were collected in 1999–2001 from brack- dresses this gap in knowledge by examining the genera ish lagoons and estuaries, brackish inland seas, and fresh- Paramysis and Limnomysis. Not only is Paramysis the most water ponds and lakes along the northwestern Black Sea speciose of the nine Ponto–Caspian mysid genera, but it also coast and in the Caspian Sea (Fig. 1). The samples were contains species such as Paramysis kroyeri, which occurs in sorted and preserved in 90% ethanol shortly after collection. salinities ranging from fresh–brackish coastal lakes (salinity < The amphipod Gammarus lacustris and the mysids Tena- 4‰) to the intertidal and subtidal zones of the Black Sea gomysis australis and Mysis relicta were used as outgroups (salinity = 18‰). in the first phase of phylogenetic analyses. To test the mono- The Ponto–Caspian amphipods belong largely to the fami- phyly of the Ponto–Caspian gammaroids, we included 16 lies Gammaridae, Pontogammaridae, and Corophiidae, which additional taxa belonging to four gammaridean families are each represented by several speciose genera (C|r|uÕu (Acanthogammaridae, Gammaridae, Hyalellidae, and Cran- 1943; Barnard and Barnard 1983; Martin and Davis 2001). gonyctidae). These more inclusive phylogenies were rooted The morphological radiation of Ponto–Caspian amphipods using the isopod Glyptidotea lichtensteini. Most amphipod has been linked to their fossorial adaptations because most taxa were represented by several populations in the phylo- species are burrowers. Although a general evolutionary trend genetic analyses of the cytochrome c oxidase subunit I towards increased specialization for burrowing is evident, (COI) gene, with samples from both the Black and Caspian the phylogenetic affinities among Ponto–Caspian gammarids seas. A phylogeographic survey was also conducted for the are unclear. It has been suggested that the nonfossorial genus mysids Limnomysis benedeni and Paramysis kroyeri at sites Echinogammarus is primitive because its gnathopods resem- within the Black Sea region. ble those of the Gammarus group (Barnard and Barnard 1983). Dikerogammarus is thought to be derived from the DNA extraction, amplification, and sequencing Ponto–Caspian Echinogammarus lineage, since its first Phylogenies were constructed using two mitochondrial gnathopod lacks the palmar spination typical of Echinogam- genes: COI and 16S ribosomal RNA (rRNA), and one nuclear marus while retaining the Gammarus type of first antenna gene, 28S rRNA. The primer pairs LCOI490 (5′-GGT- (Barnard and Barnard 1983). Other genera such as Obeso- CAACAAATCATAAAGATATTGG-3′) and HCO2198 (5′- gammarus and Pontogammarus share additional derived TAAACTTCAGGGTGACCAAAAAATCA-3′) (Folmer et al. characters such as setae on the bases of periopods 5–7 and 1994), 16Sar (5′-CGCCTGTTTATCAAAAACAT-3′)