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A Review of Gammaridae (Crustacea: Amphipoda): the Family Extent, Its Evolutionary History, and Taxonomic Redefinition of Genera

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A Review of Gammaridae (Crustacea: Amphipoda): the Family Extent, Its Evolutionary History, and Taxonomic Redefinition of Genera Zoological Journal of the Linnean Society, 2016, 176, 323–348. A review of Gammaridae (Crustacea: Amphipoda): the family extent, its evolutionary history, and taxonomic redefinition of genera ZHONGE HOU1 and BORIS SKET2* 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2Department of Biology, Biotechnical Faculty, University of Ljubljana, PO Box 2995, Ljubljana SI-1001, Slovenia Received 30 March 2015; revised 22 June 2015; accepted for publication 24 June 2015 By molecular analysis of a high number of gammarids, including 29 out-group genera, we could assure the monophyly of Gammaridae. To avoid the paraphyly of the family, we propose the omission of Pontogammaridae, Typhlogammaridae, and all Baikalian families. Similarly, the genera Fontogammarus, Sinogammarus, Lagunogammarus, Pephredo, Neogammarus, and Laurogammarus may be cancelled. But, tens of Baikal genera, nested within Gammarus, are so diverse that they must be retained, although rendering Gammarus paraphyletic. Besides we propose the polyphyletic Echinogammarus–Chaetogammarus group to be divided into monophyletic genera Echinogammarus s. str., Homoeogammarus, Parhomoeogammarus, Marinogammarus, Relictogammarus gen. nov., Chaetogammarus, and Trichogammarus gen. nov. These solutions made it possible to complete the first analysis of the family evolu- tion in light of its phylogeny. Perimarine clades are mainly basally split clades, whereas in some ancient lakes extremely rich endemic faunas had developed polyphyletically. The troglobiotic Typhlogammarus group from Dinarides and Caucasus formed a monophylum, whereas the troglobiotic assemblage of Gammarus species is highly polyphyletic. Reduction of the uropod III endopodite, which classically distinguishes between the genera Gammarus and Echinogammarus, appeared to be highly polyphyletic. Protective dorsal pleonal projections occur scattered across the family and beyond, whereas lateral projections were limited to species of ancient lakes, so both structures were polyphyletic. The evolutionary history of Gammaridae was investigated with ten different calibration schemes, which produced incompatible results; however, the most probable scenario is a late rise of the family, which can only explain the absence of Gammaridae species around the Indo-Pacific. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016 doi: 10.1111/zoj.12318 ADDITIONAL KEYWORDS: ancient lakes – molecular – phylogeny – radiation – subterranean – taxonomy – time estimation. INTRODUCTION They may occur in dense masses of over 4000 indi- viduals (Davey et al., 2006), or 1.5 g dry weight per The mainly centimetre-sized crustacean species ha- m2 (Mortensen, 1982), below stones and fallen leaves. bitually labelled as ‘gammarids’ or ‘Gammaridae’ are Several hundreds can be taken with one pull of the very common inhabitants of nearly the whole Holarctic hand net. Gammarids are one of the most conspicu- area (except the south-west of North America), where ous animal groups (with hundreds of species) in the they inhabit mainly springs, but also rivers, lakes, ancient lake Baikal (Bajkal, Bajkalskoe ozero). On the coastal lagoons, and the marine littoral zone. Spring other hand, they are only locally present and not very stretches of streams may be literally crowded by them. abundant in subterranean waters. Gammarids are very important constituents of food chains in running waters, and are even being dried and commercially offered as *Corresponding author. E-mail: [email protected] fish food for aquaria or fisheries. A journal issue was © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016, 176, 323–348 323 324 Z. HOU AND B. SKET devoted to the biology of Gammarus recently (Gerhardt, Crangonyctidae, and some other ‘crangonyctoid’ groups, Bloor & Mills, 2011). Anisogammaridae, Phreatogammaridae, and some other Throughout the history, the concept of gammarids southern groups, the Ponto-Caspian Pontogammaridae has varied remarkably. At the beginning of the 20th and some Baikalian families, and the Bogidiellidae ob- century, Stebbing (1906) divided Amphipoda into three tained family status. Moreover, from the morphologi- legiones (Gammaridea, Hyperiidea, and Caprellidea), cally exceedingly diverse Baikalian group of gammarids with Gammaridea comprising all amphipods with head the Russian authors Kamaltynov (1999a) and Tahteev not fused with the first pereonite and with a developed (2000) defined some additional families. maxilliped palp. There were 41 families included in In their most recent morphologically based and Gammaridea, whereas the family Gammaridae includ- cladistically elaborated study, Lowry & Myers (2013) ed 52 genera. Besides the obligatory Gammarus and erected the suborder Senticaudata, including the Echinogammarus, among them were also Crangonyx, infraorder Gammarida Latreille, the parvorder Niphargus, Melita, Maera, Phreatogammarus, prob- Gammaridira Latreille, and the only superfamily ably all Baikalian genera and Ponto-Caspian genera. Gammaroidea Latreille. Beside the family Gammaridae Evidently, virtually the same conception has been ac- Latreille, this superfamily contains some other cepted by Chevreux & Fage (1925) with their ‘S. O. groups of interest. These are the Baikalian endemic GAMMARIENS’ and by Schellenberg (1942) with his families: Acanthogammaridae Garjajev, Baikalogam- ‘Unterordnung Gammaridea’. The splitting of these com- maridae Kamaltynov, Iphigenellidae Kamaltynov, prehensive higher taxa only really began after the Second Macrohectopidae Sowinsky, Micruropodidae Kamaltynov, World War. A review of marine gammaridean amphipods Pachyschesidae Kamaltynov, Pallaseidae Takhteev, the (Barnard, 1969) divided the suborder into informal sec- Ponto-Caspian Pontogammaridae Bousfield, and the tions A–H, but stopped short of naming formal taxa Dinaric-Caucasian troglobiotic Typhlogammaridae between the suborder and family level. In their fol- Bousfield. This is the assemblage that we will call here lowing review of freshwater amphipods Barnard & ‘gammarids’ or ‘Gammaridae’, following the tree in Hou, Barnard, (1983) even went a step back, dissolving es- Sket and Li (2014: Fig. S1). tablished families and treating the gammaroid amphipods A molecular study by MacDonald, Yampolsky & Duffy only by groups appropriate for identification, either mor- (2005), devoted mainly to amphipods from the lake Baikal, phologically or by distribution areas. was very elucidating. Besides the in-group Baikalians, Bousfield was very active in building a phyletic this study also included quite a number of gammaroids system. First, he divided Gammaridea into six from the out-group. They show that all Baikalian and superfamilies and 24 families (Bousfield, 1977). Later, Ponto-Caspian taxa considered are nested within the he divided the suborder Gammaridea into 19 Gammarus–Chaetogammarus group, rendering it superfamilies (Bousfield, 1982, 1983). Within the su- paraphyletic, probably even polyphyletic. On the other perfamily Gammaroidea he formulated and analysed hand, the few representatives of Anisogammaridae split eight polytypic and two unnamed monotypic ‘family basally, and behave as an out-group to the gammarids. groups’: Gammaridae included a number of The study by Englisch (2001), which includes a higher ‘baikalianized’ species; Metohia group (hypogean large number of amphipod families (but with each family gammarids) should be dismembered and mainly placed represented by very few genera) gave a stepwise tree into Gammaridae; Pontogammaridae; the parasitic with the Gammarus–Chaetogammarus as one of the Cardiophilus group and Iphigenella group should distal branches, including also a representative of the be retired, and their species placed into Baikalian fauna (Parapallasea). Pontogammaridae and Acanthogammaridae, respec- Englisch (2001) was also a base for the attempt to tively; Acanthogammaridae (Baikal group) are a hetero- define the family by Hou et al. (2014), where the afore- geneous group of Baikal inhabitants, not included into mentioned Baikalian, Dinaric-Caucasian, and Ponto- Gammaridae; Anisogammaridae are ‘an excellent cluster’ Caspian families are clearly nested within Gammaridae. but were rejected as a taxon, mainly for their (at that Unfortunately, a paper by Browne, Haddock & Martindale time!) paucity. As a result of these controversies, Martin (2007) noticed later, although dealing with hyperiids, & Davis (2001) wrote: ‘The Amphipoda, despite a large has cast some doubts on our decision in delimiting the number of dedicated workers and numerous pro- family. This resulted in the present attempt to verify posed phylogenies and classificatory schemes, remain the monophyly of the family by the inclusion of a richer to a large extent an unresolved mess’. So, they only out-group set. Moreover, this is an appropriate occa- shelled one additional, small suborder (Ingolfiellidea), sion for rethinking the evolutionary history of the family. whereas the suborder Gammaridea remained other- Thus, the monophyly of the group will be again proven wise the same. The family Gammaridae suffered a great in this study, and some hypotheses about its morpho- transformation, as the suborder is divided here into logical development, and geographical and phylogenetic ∼125 families. Of the freshwater groups, Gammaridae, splitting, will be formulated. The taxonomy of the family © 2015 The Linnean Society of London, Zoological Journal
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