Taxonomy and genetic divergence of Paranoplocephala kalelai (Tenora, Haukisalmi et Henttonen, 1985) (Cestoda, Anoplocephalidae) in the grey-sided vole Myodes rufocanus in northern Fennoscandia Voitto Haukisalmi*, Lotta M. Hardman, Jukka Niemimaa and Heikki Henttonen Finnish Forest Research Institute, Vantaa Research Unit, PO Box 18, FI-01301 Vantaa, Finland Abstract Paranoplocephala kalelai (Tenora, Haukisalmi et Henttonen, 1985) is an anoplocephalid cestode that primarily parasitizes the grey-sided vole Myodes rufocanus (syn. Clethrionomys rufocanus) in northern Fennoscandia. In a preliminary molecular phy- logenetic analysis, the cytochrome oxidase I (mtDNA) sequences of P. kalelai formed two divergent sublineages originating from two different localities in northern Finland and northern Norway. The present data confirm the existence of two strongly supported clades and show that their geographic distributions are overlapping in northernmost Finland. Relatively deep genet- ic divergence and coexistence of the two main clades at one of the localities suggest that the material may include two biolog- ical species. However, because the specimens representing the two mtDNA clades of P. kalelai are not morphometrically suf- ficiently differentiated and because the mtDNA clade of the specimens from the type locality is unknown, they are not assigned to different species. Comparison with the existing phylogeographic data of M. rufocanus suggests that the genetic structure of this host-specific cestode reflects the glacial and post-glacial history of its primary host. A redescription is presented for P. kale- lai. Keywords Cestoda, Anoplocephalidae, Paranoplocephala kalelai, Rodentia, Myodes rufocanus, cytochrome oxidase I, mtDNA *Corresponding author: voitto.haukisalmi@metla.fi Introduction Paranoplocephala kalelai (Tenora, Haukisalmi et Henttonen, 1985) is an anoplocephalid cestode of the grey-sided vole Myodes rufocanus (syn. Clethrionomys rufocanus), and, less frequently, of the bank vole Myodes glareolus (syn. Clethrio- nomys glareolus), in northernmost Fennoscandia (Tenora et al. 1985, Haukisalmi et al. 1987). The molecular phylogenet- ic analysis of Haukisalmi et al. (2004) and Wickström et al. (2005) confirmed the status of P. kalelai as an independent species, and showed that P. kalelai belongs to Paranoploce- phala Lühe, 1910 s. str., a monophyletic assemblage including the type species P. omphalodes (Hermann, 1783). The main morphological differences between P. kalelai and the related, Nearctic Paranoplocephala macrocephala (Douthitt, 1915) have been described by Haukisalmi and Henttonen (2003). Most of the species representing Paranoplocephala s. str. parasitize Microtus spp. in the Holarctic region (Tenora et al. 1999, Haukisalmi et al. 2004); P. kalelai is the only species within this clade known to be specific to the Myodes voles ear- lier assigned to Clethrionomys (for the taxonomy of these vole genera, see Carleton and Musser 2005). The probable sister species of P. kalelai is Paranoplocephala jarrelli Haukisal- mi, Henttonen et Hardman, 2006, a Holarctic parasite of the root/tundra vole Microtus oeconomus and other northern Mi- crotus species (Haukisalmi et al. 2004, 2006). These facts suggest that P. kalelai has speciated through a shift from M. oeconomus to M. rufocanus in northern Europe. In an earlier molecular phylogenetic analysis (Haukisalmi et al. 2004), the four cytochrome oxidase I (COI) sequences (mtDNA) of P. kalelai formed two divergent sublineages, which occurred at two different localities in northern Finland and northern Norway. Because of the high genetic distance between the subclades, they may be regarded as independent species providing they exhibit consistent morphological dif- ferences. In the present study, extended morphometric and Stefañski DOI: 10.2478/s11686-007-0043-y © 2007 W. Stefañski Institute of Parasitology, PAS Acta Parasitologica, 2007, 52(4), 335–341; ISSN 1230-2821 Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Voitto Haukisalmi et al. molecular data sets are analysed to assess whether two mor- phologically identifiable groups exist within P. kalelai corre- sponding to the two mtDNA clades. Because many important details (e.g. the structure of the early uterus) were missing in the original description, a redescription is presented for P. ka- lelai. Materials and methods Four specimens of P. kalelai used in the preliminary analysis of Haukisalmi et al. (2004) and three additional specimens were sequenced for the mitochondrial cytochrome oxidase I (COI) gene (mtDNA). For the extraction, amplification and sequencing of DNA, see Wickström et al. (2003, 2005) and Haukisalmi et al. (2004). The GenBank numbers for the COI sequences are given in Table I and Figure 1. Five of the sequenced specimens originated from M. rufocanus from Kilpisjärvi (69°03´N, 20°55´E) in north-western Finnish Lapland and two from the same host species from Narvik (68°28′N, 17°26′E) in northern Norway (the two specimens from Narvik were erroneously reported as originating from Myodes glareolus in Haukisalmi et al. 2004). Sequenc- es of P. kalelai (641 bp) were aligned using Clustal X (Thomp- son et al. 1997) with sequences of P. jarrelli, P. omphalodes, Andrya rhopalocephala (Riehm, 1881) and Neandrya cuni- culi (Blanchard, 1891) (Fig. 1). A neighbour-joining distance phylogram was constructed in PAUP* (version 4.0 b10, Swof- ford 2002) using Kimura 2-parameter distances. Bootstrap support for the topology was estimated through 10000 repli- cates. The cestodes used for morphology were fixed flat (without pressure) in 70% ethanol, stained with Mayer’s haemalum, Semichon’s acetocarmine or iron-acetocarmine, cleared in eu- genol and mounted in Canada balsam. Representative speci- mens (whole-mounts) of P. kalelai have been deposited in the Museum of Southwestern Biology, University of New Mex- ico, USA (MSB), the Harold W. Manter Laboratory of Par- asitology, Nebraska State Museum, USA (HWML), and the Hungarian Natural History Museum, Budapest (HNHM) (Table I). The material consisted of 33 gravid or pregravid speci- mens from M. rufocanus identifiable as P. kalelai, originating from Kilpisjärvi (N = 23), Pallasjärvi (68°03′N, 24°09′E, N = 6) and Inari (68°54´N, 27°05´E, N = 2) in Finnish Lapland, and Narvik (N = 2) in Norway. Twelve additional, poorly stained and/or contracted gravid specimens were used for the measurement of egg length only. The holotype and paratype specimens of P. kalelai from M. rufocanus from Pallasjärvi, deposited at the Finnish Museum of Natural History (Zool- ogy), Helsinki (nos. 20500 and 20501 + 20502, respectively), were not included in the morphometric analysis. The morphometric analysis was performed on eight spec- imens representing the “Narvik” (N = 3) and “Kilpisjärvi” (N = 5) mtDNA clades (below). The analysis included 15 abso- lute measurements of strobila, scolex, suckers, eggs, and var- ious internal organs. Width of the ovary, vitellarium and ven- tral longitudinal osmoregulatory canals, number of testes, length of the cirrus sac, and diameter of the seminal recepta- cle were recorded from 1–4 mature proglottids from each specimen. The maximum dimensions of the cirrus sac, semi- nal receptacle and ventral longitudinal canals were also re- 336 Œl¹ski Table I. Accession and GenBank numbers for the specimens of Paranoplocephala kalelai from Myodes rufo- canus used in the morphometric analysis and molecular phylogenetic analysis. “Narvik” and “Kilpisjärvi clades” refer to the two mtDNA (COI) clades (see Fig. 1). See Materials and methods for abbreviations of museums used for the deposition of mounted voucher specimens Clade Accession numbers for mounted GenBank numbers for COI Locality voucher specimens sequences Narvik clade Kilpisjärvi, Finland HNHM 67421 EF583963 Narvik, Norway – AY181513 Narvik MSB Endo 23 AY189959 Kilpisjärvi clade Kilpisjärvi – EF583961 Kilpisjärvi MSB Endo 28 EF583962 Kilpisjärvi MSB Endo 26 AY181511 Kilpisjärvi MSB Endo 27 AY181512 Clade unknown Kilpisjärvi HWML 16698 – Kilpisjärvi HWML 16699 – Kilpisjärvi HNHM 67420 – Kilpisjärvi MSB Endo 30 – Pallasjärvi, Finland MSB Endo 29 – Pallasjärvi* MSB Endo 24 – Inari, Finland MSB Endo 25 – *Host Myodes glareolus. Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Taxonomy and genetic divergence of Paranoplocephala kalelai corded from each strobila. In addition, 8 relative measurement were calculated: the length/width ratio of mature and gravid proglottids, dimensions of the ovary, vitellarium, cirrus sac and seminal receptacle in relation to the width of the corre- sponding mature proglottid, and the diameter of suckers and minimum width of the neck in relation to the width of the scolex. Each of these variables was compared between spec- imens representing the two mtDNA clades (below). Because of the small number of specimens and measurements, no sta- tistical methods were used in this comparison. All measure- ments are in millimetres. Results The seven COI sequences of P. kalelai formed two highly sup- ported clades (Fig. 1), corroborating the preliminary results of Haukisalmi et al. (2004). However, the present data showed that the “Narvik clade” is not restricted to that particular local- ity, and that the “Narvik clade” and “Kilpisjärvi clade” co- occur at Kilpisjärvi (Table I). The pairwise Kimura 2-param- eter distance between the two clades was 0.037, which is less than the corresponding distances between the other species of Paranoplocephala s. str. (0.063–0.116, mean 0.0849, n = 10) (Haukisalmi et al. 2004). Both clades included supported sub- clades. Among the 23 morphometric variables used, only three were nearly non-overlapping between the two mtDNA clades, i.e. the relative width of the ovary, egg length and maximum length of the seminal receptacle (Table II); the remaining 20 measurements overlapped considerably. The number of sig- nificant differences is barely more than the number of signif- icantly different variables expected by chance alone (i.e. 1–2). Moreover, the egg length is based on only two specimens from each clade. Relatively deep genetic divergence and coexistence of the two main clades at Kilpisjärvi suggest that the material may include two biological species. However, because of the small number of significant quantitative differences and absence of consistent qualitative differences, the specimens representing the two mtDNA clades are not sufficiently differentiated to assign them to different species. Moreover, the mtDNA clade of the holotype specimen of P. kalelai from Pallasjärvi, or any other specimens from the type locality, are unknown. 337 Stanis³a Fig. 1. A neighbour-joining reconstruction of partial cytochrome oxidase I (mtDNA) sequences of Paranoplocephala kalelai, P. jarrelli and P. omphalodes. Andrya rhopalocephala and Neandrya cuniculi from lagomorphs were used as an outgroup. The labels show the GenBank number and locality. Values at nodes show the percentage from 10000 bootstrap replicates Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Voitto Haukisalmi et al. Paranoplocephala kalelai (Tenora, Haukisalmi et Hent- tonen, 1985) (Figs 2 and 3) Syn.: Andrya kalelai Tenora, Haukisalmi et Henttonen, 1985 The redescription is based on 30 specimens from Myodes rufocanus from Finnish Lapland. The mean and number of measurements (n) are given in parentheses after the range, and the deviating maximum values of the original description (Te- nora et al. 1985) are shown in brackets. Description: Fully developed strobila 95–167 [191] (130, n = 17) long and relatively thin; maximum width 0.98–2.06 [2.3] (1.55, n = 20), attained in pregravid or gravid proglottids. Number of proglottids 300–350 (n = 5). Scolex 0.60–0.97 [1.16] (0.73, n = 22) wide, with protruding, crateriform suck- ers usually directed anteriorly; width of suckers 0.28–0.36 [0.40] (0.325, n = 22) or 37–54% (45%, n = 22) of scolex width. Neck 0.3–0.7 (0.51, n = 18) long and usually very nar- row: 0.13–0.31 (0.19, n = 23) or 17–43% (26%, n = 22) of scolex width. Proglottids craspedote, but velum very short or absent in well-relaxed specimens. Length/width ratio 0.20 –0.65 (0.36, n = 36) in mature proglottids, increasing mark- edly in gravid proglottids (0.43–1.02, 0.63, n = 21). Genital 338 Roborzyñski rosbœŸæv fjad kadsææ¿æ Fig. 2. Scolex and mature proglottids of Paranoplocephala kalelai from Myodes rufocanus: A – scolex, Kilpisjärvi, Finland (“Kilpisjärvi clade”). B – scolex, Kilpisjärvi (“Narvik clade”). C – mature proglottid, Pallasjärvi, Finland (mtDNA-clade unknown). D – mature proglot- tid, Kilpisjärvi (“Kilpisjärvi clade”). E – mature proglottid, Narvik, Norway (“Narvik clade”). F – terminal genital ducts, Kilpisjärvi (mtDNA- clade unknown). Scale bars = 0.20 mm (A, D, E), 0.30 mm (B, C), 0.10 mm (F) Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Taxonomy and genetic divergence of Paranoplocephala kalelai pores opening in posterior half of proglottid margin. Genital pores irregularly alternating, exceptionally unilateral or with single change per strobila; in specimens with multiple chang- es on average 13.3 proglottids in each unilateral set or 8.5 changes per 100 proglottids. Ventral longitudinal osmoregulatory canals 0.015–0.085 (0.048, n = 40) wide in mature proglottids, maximum width (0.05–0.11, 0.08, n = 22) attained usually in pregravid or gravid proglottids. Ventral longitudinal canals connected by transverse canals measuring 0.014–0.030. Dorsal longitudinal osmoregulatory canals 0.011–0.020 wide, lateral to ventral canals. Genital ducts passing dorsally across longitudinal osmoregulatory canals and nerve cord. Testes 24–38 (29.6, n = 37) in number, forming compact group extending from antiporal to poral ventral osmoregula- tory canal, often overlapping former canal dorsally, but not extending across it. Testes overlap ovary, often in contact with antiporal lobe of vitellarium. Diameter of testes 0.050–0.075. Cirrus sac 0.15–0.23 (0.19, n = 40) long and 0.050–0.095 (0.070, n = 39) wide in mature proglottids, elongate, shallow constriction sometimes present at its proximal third. Length of cirrus sac increases marginally in postmature proglottids; max- imum length 0.18–0.25 (0.21, n = 23). Muscle layers of cir- rus sac poorly developed. Cirrus sac overlaps ventral longitu- dinal canal or extends across it; rarely non-overlapping with ventral canal. Ductus cirri short, usually straight, with minute spines in its distal part. Internal seminal vesicle initially spher- ical or ovoid, elongate when filled with sperm, filling up to 2/3 of cirrus sac length. External seminal vesicle fairly long, usu- ally looped, covered by loose, poorly stained cell layer. Vagina 0.11–0.16 (0.14, n = 12) long or 57–89% (77%, n = 12) of cirrus sac length, running posteriorly or postero-ven- trally to cirrus sac. Walls of vagina formed by dense layer of large cells; this cell layer thickens distally, merging with cell layer surrounding genital atrium. Distal vaginal tube lined in- ternally by delicate microtriches (seen best in sections); vagi- nal tube widening distally. Seminal receptacle 0.10–0.19 (0.14, n = 24) long and 0.07–0.13 (0.10, n = 24) wide in mature proglottids; asymmetrically elongate, pyriform or ovoid when filled with sperm. Maximum length of seminal receptacle (0.18–0.28, 0.23, n = 24) attained in postmature proglottids. Vitellarium asymmetrically bilobed, 0.14–0.25 (0.19, n = 40) 339 Fig. 3. Uterine development in Paranoplocephala kalelai from Myodes rufocanus from Kilpisjärvi, Finland: A – early uterus in a mature proglottid (“Kilpisjärvi clade”). B – fully developed uterus in a pregravid proglottid (mtDNA-clade unknown). C – fully gravid terminal proglottids (mtDNA-clade unknown). Scale bars = 0.20 mm (A), 0.30 mm (B, C) Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Voitto Haukisalmi et al. wide and 0.08–0.19 (0.12, n = 37) long, positioned usually slightly porally with respect to mid-line of ovary and proglot- tid (index of asymmetry 0.38–0.51, 0.44, n = 40). Ovary large (width 0.26–0.51, 0.37, n = 38; length 0.15–0.27, 0.21, n = 34), coarsely lobed, positioned medially, usually covering whole space between ventral longitudinal canals, often slight- ly overlapping them. Uterus appears in early mature proglottids as transverse, finely reticulated band positioned anteriorly and ventrally to other organs and extending across longitudinal osmoregula- tory canals bilaterally. Lateral ends of early uterus extend more posteriorly than central part; early uterus does not mark- edly overlap ovary. Fully developed uterus covering most of medulla, with few anterior, posterior and lateral sacculations; internal structures simple. Eggs 0.030–0.045 (0.038, n = 214) long and 0.025–0.036 (0.028, n = 47) wide, spherical or slight- ly ovoid in surface view, usually slightly citriform in side view. Pyriform apparatus present. Discussion Paranoplocephala kalelai is the most common tapeworm of M. rufocanus in northern Fennoscandia, its overall prevalence ranging between 21–27%. However, the prevalence may reach 90% in adult, overwintered males (Haukisalmi et al. 1987). Paranoplocephala kalelai, or morphologically corresponding cestodes, have not been reported outside northern Fennoscan- dia, including the extensive study Yushkov (1995) from north- western Russia. The endemicity of P. kalelai suggests that the shift from M. oeconomus and subsequent divergence in M. ru- focanus have taken place in north-western Eurasia. The Hol- arctic P. jarrelli, the probable precursor of P. kalelai, present- ly has an overlapping distribution with the latter species in northern Fennoscandia. Paranoplocephala kalelai is the only host-specific hel- minth of M. rufocanus in the western part of its range (Hau- kisalmi et al. 1987). In Central and eastern Siberia, M. rufo- canus is parasitized by another host-specialist cestode, Para- noplocephala buryatiensis Haukisalmi, Hardman, Hardman, Laakkonen, Niemimaa et Henttonen, 2007 (see Haukisalmi et al. 2007), and in Hokkaido (Japan) by Anoplocephaloides den- tatoides Sato, Kamiya, Tenora et Kamiya, 1993, also a host- specific, endemic anoplocephalid cestode of the grey-sided vole (Sato et al. 1993). Interestingly, the three known host- specific anoplocephalid cestodes of M. rufocanus have non- overlapping distributions. The pronounced genetic structure of P. kalelai suggests that its glacial and postglacial history differs from those of the other northern European Paranoplocephala and Anoploce- phaloides species of voles (Wickström 2004, L.M. Hardman et al., unpubl.). The presence of two divergent clades within P. kalelai may due to isolation of M. rufocanus at least in two glacial refugia, and subsequent recolonization and spatial overlap of the diverged populations. Some rodents have recol- onized Fennoscandia via two main routes, i.e. through a peri- odical isthmus in present-day Denmark and southern Sweden (western route), and from the south-east through present-day Finland (Jaarola et al. 1999), but there are no hypotheses or data on the post-glacial colonization of M. rufocanus into northern Fennoscandia. The oldest fossils of M. rufocanus are from Middle Pleistocene from Japan and the Baikal area, which led Chaline and Graf (1988) to propose that M. rufo- canus probably diverged in the Far East ca. 0.7 Mya. To our knowledge, no fossils of M. rufocanus have been found in western Eurasia. There exists a single spatially extensive molecular phy- logenetic data set of M. rufocanus, i.e. the cytochrome b (mtDNA) sequence data of Cook et al. (2004), consisting of 13 specimens of M. rufocanus from its western- and eastern- most populations. These data do not give unambiguous sup- port for the monophyly of M. rufocanus; in fact, the grey- sided vole may be paraphyletic with respect to Myodes regu- lus (syn. Eothenomys regulus) and Myodes smithii (syn. Phau- lomys smithii) from Korea and Japan, respectively. However, there are two strongly supported monophyletic groups with- in M. rufocanus, i.e. a Japanese clade and another, widely dis- tributed clade, spanning from Finnish Lapland and Kola Pen- insula (Russian Federation) in the west to Magadan (Russian Federation) in the east. Within the latter clade, there is a strongly supported western subclade at Kilpisjärvi and on the Kola Peninsula. These data also show that two separate sub- lineages of M. rufocanus co-occur at Kilpisjärvi. Thus, the two main lineages of P. kalelai may have di- verged as a response to a corresponding split in its primary host. No divergence time estimates are available for M. rufo- 340 Table II. The morphometric variables that were completely or nearly non-overlapping between the two mtDNA clades of Paranoplocephala kalelai. The twenty other absolute and relative measurements (see Materials and meth- ods) were widely overlapping between the clades Narvik clade (N = 3) Kilpisjärvi clade (N = 5) n range (mean) n range (mean) Ovary, relative width 5 0.54–0.62 (0.59) 11 0.44–0.55 (0.49) Egg, length 18 0.040–0.045 (0.042) 12 0.035–0.040 (0.036) Seminal receptacle, max. length 2 0.20–0.25 3 0.18–0.20 N – number of specimens examined, n – number of measurements. Brought to you by | Metla Finnish Forest Research Institute Authenticated Download Date | 7/12/17 7:28 AM Taxonomy and genetic divergence of Paranoplocephala kalelai canus, but the deepness of the cestode divergence suggests that it probably predates the latest glacial cycle and may have occurred repeatedly. In the absence of fossils and comprehen- sive phylogeographic data for the western populations of the grey-sided vole, the possible glacial refugia of M. rufocanus and P. kalelai cannot, however, be identified. Although the existing data on the phylogeography of P. ka- lelai and M. rufocanus are scanty, they suggest that the genet- ic structure of this host-specific cestode reflects the glacial and post-glacial history of its host. However, the patterns of host-anoplocephaline cestode coevolution may actually be complex and include shifts of parasites to alien host lineages and other deviations from the assumption of parasite-host co- phylogeny (Haukisalmi et al. 2004, Hu et al. 2005, Wickström et al. 2005). Acknowledgements. LMH is supported by the Finnish Academy (a postdoctoral research grant no. 108372). Joe Cook (MSB), Scott L. Gardner (HWML) and András Gubányi (HNHM) kindly helped in the deposition and examination of museum specimens. Eric P. Ho- berg and J. Cook provided the specimens of Paranoplocephala jar- relli collected in connection with the Beringian Coevolution Project. References Carleton M.D., Musser G.G. 2005. Order Rodentia. In: (Eds. D.E. 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