Systematic analysis of the caridean shrimp superfamily Pandaloidea (Crustacea: Decapoda) based on molecular and morphological evidence

Highlights

• The first molecular phylogeny of the caridean Pandaloidea is reconstructed.

• Genetic data from eight markers are generated for most Pandaloidea genera.

• Thalassocarididae should be considered a junior synonym of Pandalidae.

• Synapomorphies are recovered for the major clades.

Abstract

One of the systematically controversial superfamilies in Caridea is the predominately deep-sea or cold water Pandaloidea, largely because this species-rich group of nearly 200 species in 25 genera exhibits a very high diversity of body forms and ecology. Although the relationships amongst the taxa within Pandaloidea have been repeatedly discussed based on morphology, no comprehensive molecular phylogeny exists. In this study, we present the first molecular phylogeny of the group, based on a combined dataset of two mitochondrial (12S and 16S rRNA) and six nuclear (ATP synthase β-subunit, enolase, glyceraldehyde-3-phosphate dehydrogenase, histone 3, phosphoenolpyruvate carboxykinase and sodium–potassium ATPase α-subunit) markers, based on 62 species (about 1/3 of known biodiversity) in 22 genera (88% of genera) of two pandaloid families (Pandalidae, Thalassocarididae) and outgroups from seven other caridean families. With generally high support, the relationships within the clade are fully resolved. Pandalidae is shown to be paraphyletic with Thalassocarididae deeply nested within as a monophyletic group, and the latter is herein considered to be a synonym of Pandalidae. Five major clades are recovered, with the shallow water genera Anachlorocurtis, Chlorocurtis, Chlorotocella and Miropandalus forming a sister clade to the remaining genera. At the genus level, the phylogeny indicates Plesionika, Heterocarpus and Pandalus to be not monophyletic. The validity of Pandalopsis, Stylopandalus and Calipandalus is challenged and these genera are considered herein to be junior synonyms of Pandalus (Pandalopsis) and Plesionika (Stylopandalus and Calipandalus). Although not fully resolved, some evidence potentially considers Nothocaris to be a valid genus. Ancestral State Reconstruction successfully recovered 15 synapomorphies for the major clades, with 11 of them reported to be of systematic significance for the first time.

Introduction

Amongst the species-rich caridean shrimps (Infraorder Caridea, > 3500 species; De Grave and Fransen, 2011), the family Pandalidae is of major economic importance (Holthuis, 1980, Wicksten, 2010). Northern Shrimp (Pandalus borealis) and other pandalids (e.g. Heterocarpus reedi) account for over 48% of worldwide, shrimp capture fisheries (FAO, 2014). The family also displays a very high morphological and ecological (although primarily in deeper or colder waters) disparity. Together with the species-poor Thalassocarididae, Pandalidae comprises the superfamily Pandaloidea, which is the fifth most species-rich superfamily within Caridea, consisting of about 200 species, distributed across 25 genera (De Grave and Fransen, 2011). Morphologically, pandaloid shrimps are characterized by a non-chelate or microscopically chelate first pereiopod, the carpus of the second pereiopod generally being subdivided, and the presence of a rather simple endopod on the male first pleopod (Holthuis, 1993). Pandaloid shrimps are also highly diverse in their biology and life-style, such as protandrous hermaphrodites in Pandalus and Pandalopsis (Butler, 1980, Komai, 1999, Bergstrom, 2000), bioluminescence in Stylopandalus and Heterocarpus (Herring, 1985), and in forming symbiotic relationships with other invertebrates (Hayashi, 1975, Bruce, 1983, Chan and Crosnier, 1991, Horká et al., 2014).

Despite their economic importance and varied ecology, many controversies remain in the higher level systematics of Pandaloidea. In an earlier classification, Holthuis (1955) grouped three families (Pandalidae, Thalassocarididae, Physetocarididae) into the superfamily Pandaloidea. Thompson (1967), while supporting Holthuis’s concept, elevated the genus Heterocarpus to the family Heterocarpodidae in a separate superfamily Heterocarpodoidea with two further non-pandaloid families. Bowman and Abele (1982) separated Physetocarididae (but without any argumentation) into its own superfamily Physetocaridoidea, followed in that by Chace, 1992, Holthuis, 1993. In contrast, in the morphological cladistic analysis of Christoffersen (1989), a superfamily Pandaloidea was recognized and considered to be comprised of seven families: Pandalidae, Plesionikidae, Dorodoteidae, Heterocarpidae (recte Heterocarpodidae Thompson), Heterocarpoididae, Physetocarididae and Thalassocarididae. Notably, some genera were transferred to the previously monotypic Physetocarididae. This classification is generally not adopted in recent classification schemes (see discussion in Holthuis, 1993). Equally, in an unpublished, morpho-cladistic study by Komai (1994a), no support was found for Christoffersen’s classification and largely the more traditional scheme of Chace, 1992, Holthuis, 1993 was recovered, although with notable problems in the classification of subordinate taxa.

Within Pandalidae itself, systematic controversies abound in the species-rich Plesionika, as well as the economically important Pandalus. Plesionika currently has 93 species (Chan, 2016, Chan et al., 2018), with several species groups proposed within the genus (Chan and Crosnier, 1991, Chan and Crosnier, 1997, Chan, 2016, Chan et al., 2018), although their true phylogenetic status remains unknown. Far from settled is also the validity of Parapandalus (see Chace, 1985, Holthuis, 1993) and Nothocaris (see Burukovsky, 1981, Chace, 1985, Chan, 2004), both currently considered as synonyms of Plesionika; as well as the relationship of the “Plesionika laevis” species group to the genus Heterocarpus (see Chan and Crosnier, 1997, Yang et al., 2010). For Pandalus, uncertainty has been highlighted as to its systematic relationship with Pandalopsis, with the possibility repeatedly raised that both taxa are synonyms (Komai, 1994a, Komai, 1995, Komai, 1999, Bergstrom, 2000).

While morphological studies rarely reach consensus, molecular tools have so far only been used to address species status of selected taxa or for within-genus phylogenies (Zuccon et al., 2012, Matzen da Silva et al., 2013). Some previous studies (e.g. Tsang et al., 2008, Bracken et al., 2009, Li et al., 2011, Aznar-Cormano et al., 2015) did include pandaloids, although none resolved intra-familial issues due to limited taxon sampling (less than ten species across all studies).

In this study, using a comprehensive molecular dataset of two mitochondrial (12S rDNA, 16S rDNA) and six nuclear protein-coding markers (histone 3 (H3), sodium–potassium ATPase α-subunit (NaK), enolase, phosphoenolpyruvate carboxykinase (PEPCK), ATP synthase β-subunit (atpβ), glyceraldehyde 3-phosphate dehydrogenase (GAPDH)) from 60 species belonging to 20 pandalid genera, one species each from the two thalassocaridid genera and 11 species from seven other caridean families, we endeavor to (1) examine the monophyly of the superfamily Pandaloidea as currently perceived (sensu De Grave and Fransen, 2011); (2) test the reciprocal monophyly of the families Pandalidae and Thalassocarididae, and (3) disentangle the phylogenetic relationships among pandalid genera. In addition, ancestral state reconstruction of morphological characters was conducted to recover synapomorphies in Pandaloidea to aid in the interpretation of morphological evolution in these shrimps.