Species boundaries and phylogeographic patterns in new species of Nannoniscus (Janiroidea: Nannoniscidae) from the equatorial Pacific nodule province inferred from mtDNA and morphology Author Kaiser, Stefanie Author Kihara, Terue Cristina Author Brix, Saskia Author Mohrbeck, Inga Author Janssen, Annika Author Jennings, Robert M. text Zoological Journal of the Linnean Society 2021 2021-02-01 193 1020 1071 journal article 3729 10.1093/zoolinnean/zlaa174 a51bb380-e42b-4b8f-9b25-27925807792f 0024-4082 5639160 A68FDF1F-2825-47D8-B9CE-FEB8432896DF Genus: Nannoniscus Sars, 1870 . Nannoniscus Sars, 1870: 164 ; Hansen, 1916: 87–89; Gurjanova, 1932: 51; Menzies, 1962b: 133; Birstein, 1963: 78 ; Siebenaller & Hessler, 1981: 241 ; Kussakin, 1999: 68; Wilson, 2008: 13 ; Saetoniscus Brandt, 2002: 11 . Type species: Nannoniscus oblongus Hansen, 1916 . Species included (see also Table 3 ): Nannoniscus acanthurus Birstein, 1963 , Nannoniscus aequiremus Hansen, 1916 , Nannoniscus affinis Hansen, 1916 , Nannoniscus analis Hansen, 1916 , Nannoniscus antennaspinis Brandt, 2002 , Nannoniscus arcticus Hansen, 1916 , Nannoniscus arctoabyssalis Just, 1980 , Nannoniscus australis Vanhöffen, 1914 , Nannoniscus bidens Vanhöffen, 1914 , Nannoniscus bidens sensu Brandt, 1992 , Nannoniscus brenkei Kaiser, Brix & Jennings sp. nov. , Nannoniscus camayae Menzies, 1962 , Nannoniscus caspius Sars, 1899 , Nannoniscus cristatus Mezhov, 1986 , Nannoniscus detrimentus Menzies & George, 1972 , Nannoniscus hilario Kaiser & Kihara sp. nov. , Nannoniscus inermis Hansen, 1916 , Nannoniscus laevis Menzies, 1962 , Nannoniscus laticeps Hansen, 1916 , Nannoniscus magdae Kaiser, Brix & Jennings sp. nov. , Nannoniscus menoti Kaiser, Janssen & Mohrbeck sp. nov. , Nannoniscus menziesi Mezhov, 1986 , Nannoniscus meteori ( Brandt, 2002 ) , Nannoniscus minutus Hansen, 1916 , Nannoniscus muscarius Menzies & George, 1972 , Nannoniscus oblongus Sars, 1870 , Nannoniscus ovatus Menzies & George, 1972 , Nannoniscus pedro Kaiser, Brix & Kihara sp. nov. , Nannoniscus perunis Menzies & George, 1972 , Nannoniscus plebejus Hansen, 1916 , Nannoniscus profundus Svavarsson, 1982 , Nannoniscus reticulatus Hansen, 1916 , Nannoniscus simplex Hansen, 1916 , Nannoniscus spinicornis Hansen, 1916 , Nannoniscus teres Siebenaller & Hessler, 1981 . Figure 3. Haplotype network for COI . Sampled haplotypes are shown as solid circles with circle area proportional to the number of individuals possessing that haplotype; open circles represent unsampled haplotypes required to connect the network. The number of mutational steps between haplotypes are shown along connecting lines. The colours represent sampling locations as indicated in the legend. Species described herein are indicated with bounding boxes. Figure 4. Genetic divergence (p-distance) in relation to geographic distance in kilometres for N. menoti . Diagnosis (modified from Siebenaller & Hessler, 1981: 241 ; Wilson, 2008: 14 ): Pereonal tergites projecting laterally from pereopodal coxae; pereonites 6–7 dorsal articulation absent medially. Pleotelson distinctly shorter than pereonites 5–7 combined. Antennula with 5 segments, distal article bulbous, article 4 distal margin with ventromedial angular projection. Mandible with 3-segmented palp. Pereopods I–II equally robust. Uropods biramous or rarely uniramous. Distribution: Known records from the Arctic, Atlantic, Pacific and Southern oceans and the Caspian Sea, although likely to be globally distributed. Although few Nannoniscus species are described from the continental shelf (≥ 75 m ), they occur mainly at slope and abyssal depth, with two species recorded from the hadal Zone ( N. ovatus Menzies & George, 1972 and N. perunis Menzies & George, 1972 ; Table 3 ). Remarks: Species described herein were assigned to Nannoniscus due to the following characters: antennula article 4 distal margin with ventromedial angular projection, antennula terminal article 5 bulbous, pereopods 1 and 2 equally robust, lack of ventral articulation between pereonites 6 and 7. However, the genus Nannoniscus , thus far, is largely defined by a combination of plesiomorphic characters, such as uropods inserting posteroventrally close to the anus ( Wilson, 2008 ), defining the family Nannoniscidae , as well as synapomorphic characters, such as a bulbous terminal article of the antennula, a specialized antennula article 4 and fusion of pereonites 6 and 7 that characterize a cluster of nannoniscid genera containing Nannoniscus , Nannonisconus Schultz, 1966 , Nymphodora Kaiser, 2009 , Rapaniscus Siebenaller & Hessler, 1981 and Regabellator Siebenaller & Hessler, 1981 . Wilson (2008) states that the broad body form with laterally projecting pereonite tergites is present in all Nannoniscus species. While this is true for some species (e.g. the type species N. oblongus ), others have a slender body (body length> 4.5 times pereonite 1 width) with lateral tergites that extend only slightly, if at all (e.g. N. ovatus , N. perunis , N. menziesi , N. meteori and species described herein). Overall, the genus comprises species with diverse morphologies mostly referring to the shape of the pleotelson and the presence of a ventral spine on the female operculum and/or pereonite 7. While N. oblongus possesses a ventral opercular spine, there are several species, where a spine is overall absent (e.g. N. aequiremis , N. arctoabyssalis , N. cristatus , N. inermis ), or one occurring on the seventh pereonite ( N. australis , N. minutus , N. muscarius , N. spinicornis , N. reticulatus , N. plebejus , N. affinis , N. profundus , N. caspius ). In N. reticulatus , ventral spines are present both on the female operculum and the seventh pereonite. The presence or absence of a ventral opercular spine has been found a useful character to separate the nannoniscid genera Ketosoma and Thaumastosoma Hessler, 1970 ( Kaiser et al. , 2018 ). Equally, the position of ventral spines on pereonites 6 and 7 represents an apomorphy of Regabellator . In contrast, in Rapaniscus species , similar to Nannoniscus , the position of the ventral spines is variable, present on either pereonite 7 [ Rapaniscus crassipes (Hansen, 1916) , Rapaniscus dewdneyi Siebenaller & Hessler, 1981 ] or the operculum ( Rapaniscus multisetosus Brandt, 2002 ). Figure 5. Bayesian reconstruction of geographic location of ancestral lineages of Nannoniscus , based on sampling area of extant lineages. Brackets above and below branches list potential locations and their 95% highest posterior distributions, respectively. Further differences exist in the presence or absence of the uropodal exopodite among Nannoniscus species ; most species within the genus possess biramous uropods, while a lack a uropodal exopod is reported for two species ( N. ovatus and in one new Nannoniscus species described below). Presence of uniramous or biramous uropods has been used as a segregating character to define genera within the munnopsid subfamily Ilyarachninae ( Merrin, 2007 ) ; however, there are several genera (e.g. within Desmosomatidae , Paramunnidae ), where both character states occur ( Just & Wilson, 2007 ; Brix & Bruce, 2008 ; Kaiser & Marner, 2012 and discussion therein). Nannoniscus species described below show a gradual reduction of the exopodite (well-developed vs. minute vs. absent), thus, at least in Nannoniscus , the presence or absence of the uropodal exopodite represents a valuable character at the species, but not at the generic level [see also Brix & Bruce (2008) for desmosomatids]. Table 3. Checklist of described Nannoniscus species with information on their type locality and depth distribution

Species	Type locality	Depth (m)
N. acanthurus Birstein, 1963	NW Pacific	3941–5495
N. aequiremus Hansen, 1916	S of Jan Mayen, Arctic Ocean	885
N. affinis Hansen, 1916	SW Iceland, N Atlantic	1505
N. analis Hansen, 1916	Davis Strait, Labrador Sea	2258
N. antennaspinis Brandt, 2002	Angola Basin, SE Atlantic	5389–5415
N. arcticus Hansen, 1916	S of Jan Mayen, Arctic Ocean	75–699
N. arctoabyssalis Just, 1980	Eurasian Basin, Arctic Ocean	3970
N. australis Vanhöffen, 1914	E Antarctic	385
N. bidens Vanhöffen, 1914	E Antarctic	385
N. bidens sensu Brandt, 1992	Weddell Sea	191–257
N. brenkei Kaiser, Brix & Jennings	Eastern German licence area, CCZ	4093–4136
N. camayae Menzies, 1962	Caribbean Panama	1714
N. caspius Sars, 1899	Caspian Sea	n.a.
N. cristatus Mezhov, 1986	Gulf of Alaska, NE Pacific	3200
N. detrimentus Menzies & George, 1972	Peru-Chile-Trench, SE Pacific	3909–3970
N. hilario Kaiser & Kihara	Eastern German licence area, CCZ	4093–4259
N. inermis Hansen, 1916	Davis Strait, Labrador Sea	2258
N. laevis Menzies, 1962	SE Atlantic	4885
N. laticeps Hansen, 1916	N Iceland	552
N. magdae Kaiser, Brix & Jennings	French licence area, CCZ	5017–5024
N. menoti Kaiser, Janssen & Mohrbeck	French licence area, CCZ	4076–5024
N. menziesi Mezhov, 1986	Gulf of Alaska, USA	4800
N. meteori ( Brandt, 2002 )	Angola Basin, SE Atlantic	5389
N. minutus Hansen 1916	Davis Strait, Labrador Sea	1096
N. muscarius Menzies & George, 1972	Peru-Chile-Trench, SE Pacific	3909–3970
N. oblongus Sars, 1870	Lofoten, Iceland	219–5843
N. ovatus Menzies & George, 1972	Peru-Chile-Trench, SE Pacific	6321–6328
N. pedro Kaiser, Brix & Kihara	GSR licence area, CCZ	4093–5024
N. perunis Menzies & George, 1972	Peru-Chile-Trench, SE Pacific	4823–6281
N. plebejus Hansen, 1916	SW Iceland, N Atlantic	1505
N. profundus Svavarsson, 1982	Norwegian See, off Greenland	2475–2502
N. reticulatus Hansen, 1916	N Iceland	80–1020
N. simplex Hansen, 1916	W Iceland	1070–1505
N. spinicornis Hansen, 1916	S of Jan Mayen, Arctic Ocean	2465
N. teres Siebenaller & Hessler, 1981	NE Atlantic	4426–4435

Siebenaller & Hessler (1981) and Brandt (2002) already discussed the likely paraphyly of Nannoniscus particularly referring to “odd” species such as N. muscarius (with a strongly produced coxal spine) and N. ovatus (= uniramous uropods). However, these species are notsingle occurrences but representative for this heterogeneous group. Up to now there has been no rigorous phylogenetic assessment of all Nannoniscus species , and it is not the purpose of the present study to address this issue. Nevertheless, as a prelude, the position of N. coalescus ( Menzies & George, 1972 ) is discussed. The species had been first described as Desmosoma coalescum in the family Desmosomatidae and was later transferred to Nannoniscus by Siebenaller & Hessler, 1977 due to the bulbous terminal article of the antennula as well as fusion of pereonites 6 and 7. Our morphological analyses of the holotype alongside line drawings made by Menzies & George (1972 : p. 9.48) suggest the species belongs to Rapaniscus owing to a broadened pereopod I carpus bearing several long robust setae ( Siebenaller & Hessler, 1981 ). Therefore, N. coalescus is herein transferred to Rapaniscus .