Evolution and phylogeny of the deep-sea isopod families Desmosomatidae Sars, 1897 and Nannoniscidae Hansen, 1916 (Isopoda: Asellota)

Abstract

In the deep sea, the phylogeny and biogeography of only a few taxa have been well studied. Although more than 200 species in 32 genera have been described for the asellote isopod families Desmosomatidae Sars, 1897 and Nannoniscidae Hansen, 1916 from all ocean basins, their phylogenetic relationships are not completely understood. There is little doubt about the close relationship of these families, but the taxonomic position of a number of genera is so far unknown. Based on a combined morphological phylogeny using the Hennigian method with a dataset of 107 described species and a molecular phylogeny based on three markers (COI, 16S, and 18S) with 75 species (most new to science), we could separate Desmosomatidae and Nannoniscidae as separate families. However, we could not support the concept of the subfamilies Eugerdellatinae Hessler, 1970 and Desmosomatinae Hessler, 1970. Most genera of both families were well supported, but several genera appear as para- or even polyphyletic. Within both families, convergent evolution and analogies caused difficulty in defining apomorphies for phylogenetic reconstructions and this is reflected in the results of the concatenated molecular tree. There is no biogeographic pattern in the distribution as the genera occur over the entire Atlantic and Pacific Ocean, showing no specific phylogeographical pattern. Poor resolution at deep desmosomatid nodes may reflect the long evolutionary history of the family and rapid evolutionary radiations.

Supplementary information: The online version contains supplementary material available at 10.1007/s13127-021-00509-9.

Keywords: Abyssal; Atlantic Ocean; Henningian method; Molecular phylogeny; Taxonomy.

Fig. 1

World map indicating sampling spots for the molecular dataset. White circles indicate nannoniscids in the samples, black squares desmosomatids in the samples. Orange dots with numbers indicate nannoniscid genera where sequences of the type species are available, green and blue squares with numbers indicate desmosomatid genera where sequences of the type species are available and included in the mirrored trees (see Fig. 8)

Fig. 2

Type localities of type species of desmosomatid genera. The blue squares reflect the genetic dataset available in this study (compare Fig. 1). 1—Chelantermedia composita Brix, , 2—Chelator insignis (Hansen, 1916), 3—Cryodesma agnari Svavarsson, , 4—Desmosoma lineare G.O. Sars 1864, 5—Disparella valida Hessler, , 6—Echinopleura aculeata (G.O. Sars, 1864), 7—Eugerda tenuimana (G.O. Sars, 1866), 8—Eugerdella coarctata (G.O. Sars, 1899), 9—Mirabilicoxa gracilipes (Hansen, 1916), 10—Momedossa profunda Hessler, , 11—Oecidiobranchus plebejum (Hansen, 1916), 12—Paradesmosoma conforme (Kussakin, 1965), 13—Parvochelus russus Brix & Kihara, , 14—Prochelator lateralis (G.O.Sars, 1899), 15—Pseudomesus brevicornis (Hansen, 1916), 16—Reductosoma gunnera Brandt, , 17—Torwolia subchelatus Hessler, , 18—Whoia angusta (G.O.Sars, 1899)

Fig. 3

Type localities of type species of nannoniscid genera. The orange dots reflect the genetic dataset available in this study (compare Fig. 1). 1—Austroniscus ovalis (Vanhöffen, 1914), 2—Exiliniscus clipeatus Siebenaller & Hessler, 1981, 3—Ketosoma ruehlmanni Kaiser & Janssen, , 4—Hebefustis vafer Siebenaller & Hessler, 1981, 5—Nannoniscoides angulatus (Hansen, 1916), 6—Nannoniscus oblongus (G.O. Sars, 1870), 7—Nannonisconus latipleonus (Schultz, 1966), 8—Nymphodora fletcheri (Paul & George, 1975), 9—Panetela wolffi Siebenaller & Hessler, 1981, 10—Rapaniscus dewdenyi Sienbenaller & Hessler, 1981, Regabellator profugus Siebenaller & Hessler, 1981, 12—Thaumastosoma platycarpus Hessler,

Fig. 4

Prochelator angolensis Brenke, Brix & Knuschke, 2005 as SEM photo to illustrate a typical desmosomatid habitus. In this species, P I is forming a chelate condition using a large composed seta at the carpus (see Fig. 5J) as counterpart to the propodus. Abbrevations: A1, antennula; A2, antenna; Md, mandible; Mxp, maxilliped; 1–7, pereonites 1 to 7; PI, pereopod I; PII, pereopod II; PIII, pereopod III; PIV, pereopod IV; PV, pereopod V; PVI, pereopod VI; PVII, pereopod VII; Op, operculum; Plt, pleoteson; Ur, uropod; spine, posterolateral spine

Fig. 5

Generalized sketch drawings of main characters discussed in the main manuscript. (A) Positioning of setae on either tergite (nannoniscid character, Nannoniscus oblongus modified after Wilson, 2008) or (B) coxae (desmosomatid character: standardized Chelator specimen modified after Brix et al. (2015); (C) bulbous 5-segmented antennula modified after Wilson (2008), i.e., Nannoniscus, Rapaniscus, Regabellator, and Exiliniscus)); (D) antennula article 2 with two large articulated broom setae modified after Hessler (1970); (E, F, G) presence or absence of posterolateral spines at the pleotelson and pleotelson shape as well as degree of somite articulation is variable within nannoniscid genera (e.g., Nannoniscoides)—in (F) uropods covering anus valves (Pseudomesus); (H) dorsal row of long setae on carpus of PII (Echinopleura) modified after Brix (2007); (J) composed (unequally bifid) seta according to Hessler (1970); (K) subchelate PI of Torwolia after Brix (2007); (L) ventral rows of natatory setae at PV-VII in Eugerda modified after Park (1999); (M) shape of the fifth pereonite comparable to Torwolia creper Hessler, (here: convex); (N) shape of the fifth pereonite comparable to Prochelator hampsoni Hessler, (here: concave); (O) raptorial and enlarged PI in Eugerdella and Whoia modified after Hessler (1970); (P) chelate PI (Disparella); (Q) unspecialized PI in Mirabilicoxa/Desmosoma holding rows of composed setae. Little black arrows may focus the reader’s eye to the illustrated characters

Fig. 6

Bayesian, ultrametric, unrooted circle tree for COI. Bayesian posterior probabilities are shown only for nodes relevant to species delimitations (SDs); interior nodes are in gray. Bars in the inner three rings (gray) denote molecular SDs for the three methods as labeled. Bars in the outer black ring denote morphological species determination, with genera indicated in the legend

Fig. 7

Bayesian, ultrametric, unrooted circle tree for 16S. Format and labeling as in Fig. 4

Fig. 8

Mirrored morphological and molecular phylogenetic trees. Panel A, morphological strict consensus parsimony tree. Numbers on branches indicate steps along that branch. Panel B, molecular 2G Bayesian consensus tree. Some nodes were rotated or moved along polytomous bases to maximize vertical correspondence of taxa between the trees. Numbers on branches indicate posterior probability. Green bars show 95% confidence intervals (CI) for estimated divergence dates based on fossil calibrations, using the time scale at figure bottom. In both panels, white text indicates genera found only in that tree and asterisks mark genera for which the type species was included; orange shading denotes the Nannoniscidae, whereas blue (Eugerdellatinae) and green (Desmosomatinae) denote the two subfamilies of Desmosomatidae proposed by Hessler (1970). Panel C, estimated speciation rate through time (LTT analysis). The red line and shading show the mean and 95% CI from TESS, and the blue cloud shows the same from BAMM