The phyletic status of the Paludicola

Ian R. Ball Institute of Taxonomic Zoology, University of Amsterdam, Plantage Middenlaan 53, Amsterdam, The Netherlands

Keywords: Turbellaria, Tricladida, Paludicola

Abstract

Is the assumption of the monophyly of the Paludicola (freshwater triclads) justified? There seems little doubt on morphological grounds of the close relationship between the and the but it is difficult to connect, phylogenetically, the with these groups. A connection between the former and some of the latter has been unknowingly implied by the author in previous papers, thus raising an anomaly since this would mean that the Dugesiidae are not monophyletic. Is it possible that the Dugesiidae and the Planariidae + Dendrocoelidae have arisen independently from marine ancestors? The implications of such a speculation are examined.

Introduction continental break-up. The northwards dispersal of elements of this original fauna coincided with the The purpose of this paper is to draw attention to early disruption of Gondwanaland and after se- an anomaly in previously developed theories of the paration was well underway the subgenus Dugesia origin and distribution of freshwater triclads (Ball arose in Africa and after closure of the Tethys sea 1974a, 1977a). I have failed to resolve this anomaly dispersed northwards and throughout Palaearctis while retaining the assumption of the monophyly of (after the opening of the North Atlantic Ocean). the Paludicola, but the anomaly disappears if that The subgenus Schmidtea arose later in western assumption is dropped. Nonetheless, a proposal Palaearctis. The higher freshwater triclads, the that the Paludicola may be di- or even polyphyletic Planariidae and Dendrocoelidae, together consti- has other implications that need exploring. tuting the sister group of the Dugesiidae, arose in Palaearctis also after the closure of the Tethys sea and the elevation of the Himalayan chain. The original hypothesis In a later paper (Ball 1977a) it was argued that Schmidtea probably was not 'derived' but rather In its strict formulation (Ball 1975) the original represented the modern descendents of an origi- hypothesis has been summarised by Pielou (1980) nally widespread (Pangaean) proto-dugesiid which and by Lewis (1980). Pielao has misunderstood later differentiated vicariantly, so much of the some of the arguments and so her discussion is dispersal element of the earlier formulation could invalid. In brief, I regarded the Dugesiidae as the be abandoned. Ultrastructural studies by Gremigni most primitive family of freshwater triclads and (1979) support this alternative as does continuing proposed that they had originated south of the histological work by E.J. de Vries and myself. present day equator, in Gondwanaland, prior to For the purposes of the discussion which now

Hydrobiologia 84, 7 12 (1981). 0018-8158/81/0841-0007/$01.20. © Dr W. Junk Publishers, The Hague. Printed in the Netherlands. 8

TRICLADIDA

DIPLONEURA HAPLONEURA

TERRICOLA PALUDICOLA

4

Fig. 1. Phylogenetic relationships of the Tricladida showing the defining autapomorphies for each phyletic line (black squares). The characters are: (1) inner pharyngeal muscles intermingled, (2) anterior adhesive organ present, (3) multicellular eye-cup, (4) common oviduct opens into atrium, (5) probursal, (6) reduced cephalic duct (7) diploneuran nervous system, (8) tricladoid intestine, (9) germaria anterior in female gonads.

Table 1. Classification of the Tricladida. characters defining precisely each line are then referred to as autapomorphies for the group in I. DIPLONEURA question. 1. 1. Terricola 2. HAPLONEURA The systems outlined in Table I and Fig. I 2.1. Maricola require that there be autapomorphies defining the 2.2. Paludicola Haploneura, the Maricola, and the Planariidae, but 2.2. 1. Dugesioidea these remain to be discovered, if indeed they exist. 2.2.1.1. Dugesiidae More important for the present discussion is the 2.2.2. Planarioidea 2.2.2.1. Planariidae anomalous state of the Paludicola for if the 2.2.2.2. Dendrocoelidae Planarioidea arose in the Northern Hemisphere after the closure of Tethys then they must have closer phylogenetic relationships with some (i.e. follows the classification and sistergroup relation- northern) Dugesioidea than with others (i.e. ships that the original hypothesis require are shown southern) (Fig. 2), thus implying that there are one in Table 1 and Fig. 1. I shall refer to the Planariidae or more synapomorphies uniting some of the plus Dendrocoelidae as the superfamily Plana- Dugesiidae with the Planarioidea. In other words rioidea co-ordinate with the Dugesioidea, the latter the Dugesiidae sensu Ball 1974a are non- containing the single family Dugesiidae. monophyletic, and yet they seem to be well defined by the autapomorphy of their peculiar eye structure (Ball 1974b). If Fig. 2 is correct then there has been The anomaly secondary loss of the 'dugesiid eye' and a return to the primitive condition in the Planariidae, and In strict phylogenetic classifications, which are evolution in a new direction in the Dendrocoelidae. essential for biogeographical analysis, the members It could be claimed that the proto-dugesiid (eg. pre of each phyletic line must be united by uniquely Cura - Schmidtea) had the primitive 'maricolan derived shared features, or synapomorphies. The eye', leading direct to the Planariidae, but then it 9

MARICOLA DUGESIIDAE PLANARIIDAE DENDROCOELIDAE orthern

Fig. 2. A possible, stylised, phylogeny of the Haploneura as implied in earlier publications. For further discussion see text. would be necessary, under the vicariance hypo- the Planarioidea seem well assured by autapo- thesis (Ball 1977a), to assume a multiple origin of morphous characters (Fig. 1) but it is difficult to the complex 'dugesiid eye'. link the two, wholly or in part. The supposed autapomorphies of the Paludicola are two (Fig. 1, characters 5,6); their probursal condition and the A possible resolution of the anomaly reduced cephalic duct, lacking precerebral diverti- cula, of the intestine. These are positional The problems of the status of the paludicolan characters rather than complex structural cha- groups can be resolved by assuming that the racters and by generally accepted criteria of freshwater triclads are diphyletic. The phyletic homologous relationships (see Riedl 1978) must be relationships of the turbellarian groups, and their considered as weak defining characters. If one defining characters, have been discussed by Karling ignores them (but see below) an alternative (1974) and by Ball (1974a) for the Tricladida. phylogeny of the Tricladida could be based on Fig. Within the latter the integrity of the Dugesiidae and 3. This assumes a diphyletic origin of the freshwater

TERRICOLA MARICOLA DUGESIIDAE PLANARIIDAE DENDROCOELIDAE (nvs systm) (?) (eye) (?) (pharynx)

(ovi duct)

like marine ancestors

Fig. 3. A proposed open phylogeny of the Tricladida in which the Paludicola are diphyletic. See text. 10

triclads, and an independent origin of the Maricola, independently and severally in some marine triclads from marine proseriatelike ancestors. This ad- of the genera Probursa(Hyman 1944), Pacificides mittedly speculative view, which expresses the (Holmquist & Karling 1972) and Bdellasimilis(Ball degree of our ignorance concerning the Tricladida 1976), and with a tendency to this condition in rather than the depth of our knowledge, has many Tryssosoma (Ball 1977b). There are also retro- implications. bursal occurring in freshwaters, Rhodax (Marcus 1946), Opisthobursa (Benazzi & Gianni- ni 1973), Eviella (Ball 1977c) and Balliania(Gour- Are the Paludicola diphyletic? bault 1978) which have been variously assigned to the Paludicola and the Maricola (for discussions If the proposal of the non-monophyly of the see Ball 1977a; Gourbault 1978). It seems that there Paludicola, as indicated in Fig. 3, is accepted then are no compelling reasons for assuming the pro- this implies that there should be autapomorphies bursal condition of the Paludicola to be uniquely defining (a) the Dugesiidae, (b) the Planarioidea, derived. (c) the Planariidae, (d) the Dendrocoelidae, and not Similar arguments can be advanced concerning for (e) the Dugesiidae plus any or all of the the cephalic duct. The fact that the anterior ramus Planariidae and/or Dendrocoelidae. Conditions of the intestine does not form precerebral diverti- (a), (b) and (d) are met (Fig. 1, characters 3,4,1 cula in the Paludicola, whereas it does in the respectively); (c) is not met but then nor is it in the Maricola, has been used as a defining or diagnostic alternative schemes, wherein this same criterion is character in the appropriate group (Meixner 1928; required. Condition (e) is violated only by the two Luther 1960). Yet in the maricolan species of the weak characters (Fig. 1, characters 5,6) already family Bdellouridae this duct is reduced, whereas in discussed, and these need further consideration. some Tasmanian freshwater triclads of the genus With respect to the probursal condition we may Spathula there are marked precerebral or preo- note that this is generally accepted as having arisen cellar intestinal diverticula (Ball & Tran 1979), and A B

C D 1-ftit- Il

Fig. 4. Sections through the eyes of some turbellarians, diagrammatic. A Gnosonesima (Lecithoepitheliata), after Karling. B. Alaurina (Microstomidae) after Hyman. C. (Planariidae, Tricladida). D Dugesia (Dugesiidae, Tricladida). 11 some Australian specimens of Curapinguis exhibit they might be diphyletic (Fig. 3) not only solves the same phenomenon. The features of the cephalic certain problems but it also opens up new avenues of duct in the Paludicola, i.e. reduction, are neither enquiry if the hypothesis is to be properly tested. necessary nor sufficient for membership in the group, nor are they confined to the group. The ecological criteria separating the Maricola Implications for the Tricladida as a whole and the Paludicola have also fallen and indeed such criteria are usually of low phylogenetic value. It The open scheme presented as Fig. 3 requires, may be noted that on several southern hemisphere under the assumption that the diploneuran nervous islands, such as Tierra del Fuego, Gough Island, St. system is autapomorphous for the Terricola, that the Helena, Posession Island and Kerguelen Island, Haploneura be para- or polyphyletic. Indeed no maricolan planarians are known from freshwaters, good defining character(s) for the group has been and this is true also of one Australian marine triclad found. Moreover, the Maricola may be monophy- which is known only from freshwaters (see Ball letic or not, but hitherto no autapomorphy for the 1977b). infraorder has been discovered. The position of the One important implications remains to be dis- Terricola causes many problems if only because we cussed and this concerns the types of eyes found in know so little of phylogenetic relationships within the Dugesiidae and the Planarioidea, and their the land planarians. In Fig. I a number of alter- respective origins, for under the scheme of Fig. 3 natives are shown. Marcus (1953) considers them to they must have had separate origins. be closeto the Maricola but obviously if they have an The eye of the Dugesiidae comprises a multi- ancestor uniquely in common with the latter then the cellular pigment cup embracing numerous retinal integrity of the Haploneura must fall, and likewise if cells. In the Maricola and the Planariidae the they originated at a point between characters 5 and 6 pigment cup comprises one cell containing one to in the same Figure. The exact position of the three visual cells; the Dendrocoelidae are similar Terricola is an unsolved problem. but have numerous visual cells. An evolutionary transformation from the planariid to the dendro- coelid condition is readily evisaged but not so for References the planariid to dugesiid condition. But if the Paludicola are diphyletic then the latter has never Ball, I. R., 1974a. A contribution to the phylogeny and occurred. The single celled eye cup of the Plana- biogeography of the freshwater triclads (Platyhelminthes: & Morse, M. P. The be derived from one Turbellaria). In: Eds. Riser, N. W. riidae (Fig. 4c) perhaps could Biology of the Turbellaria. McGraw-Hill, New York, pp. like that of some of the lower Turbellaria (Fig. 4a) 339-401. and the eye of the Dugesiidae (Fig. 4d) from one Ball, I. R., 1974b. A new genus and species of freshwater like the multicellular epidermal light sensitive struc- from Australia (Platyhelminthes, Turbellaria). J. ture of some Monocelididae (Fig. 4b). In fact a Zool., Lond. 174: 149-158. Nature and formulation of biogeographical that of Fig. 4b and Ball, 1. R., 1975. condition intermediate between hypotheses. Syst. Zool. 24: 407-430. 4d is known from Spathula camara, an australian Ball, I. R., 1976. Observations on Bdellasimilis barwicki, a freshwater triclad lacking normal eyes but posses- marine triclad from Australian freshwaters (Platyhelmin- sing deeply invaginated epidermal canals which are thes: Turbellaria). Aust. Zool. 19: 95-101. surrounded by pigment granules (Ball 1977d). Ball, 1. R., 1977a. On the phylogenetic classification of aquatic suggested here would planarians. Acta zool. fenn. 154: 21-35. Elucidation of the possibilities Ball, 1. R., 1977b. La Faune Terrestre de l'lle de Sainte-Hlne perhaps best come from ultrastructural work on a 1V-2. Turbellaria. Ann. Mus. roy. Afr. centr. Zool. 220: wider range of turbellarians. 492-511. From the informationjust discussed I suggest that Ball, 1. R., 1977c. A new and primitive retrobursal planarianfrom there are no good reasons, other than tradition, for Australian freshwaters (Platyhelminthes, Turbellaria, Tri- 149-155. Paludicola to be monophyletic. This cladida). Bijdr. Dierkunde 47: believing the Ball, 1. R., 1977d. A monograph of the genus Spathula does not mean that they are not, but only that their (Platyhelminthes, Turbellaria, Tricladida). Aust. J. Zool. monophyly has not been demonstrated. Here is a Suppl. 47: 1-47. weakness in our knowledge. The suggestion that 12

Ball, I. R. & Tran, T. V. H., 1979. New freshwater triclads from Lewis, R. W., 1980. Evolution: a system of theories. Perspectives Tasmania (Platyhelminthes, Turbellaria). Bijdr. Dierkunde Biol. Med. 1980: 551-572. 49: 153-161. Luther, A., 1961. Die Tubellarienfauna Ostfennoskandiens 11. Benazzi, M. & Giannini, E., 1973. A remarkable cave planarian: Tricladida. Fauna Fennica 11: 1-42. Opisthobursa mexicana Benazzi,, 1972. Acc. Naz. Lincei, Marcus, E., 1946. Sobre Turbellaria brasileiros. Bol. Fac. Cienc. Quaderno 171: 47-54. Letr. Zool. S. Paulo 11: 5-254. Gourbault, N., 1978. Une nouvelle planaire primitive d'origine Marcus, E., 1953. TurbellariaTricladida. Inst. Parcs Nat. Congo marine, TurbellariE Triclade de Polynesie. Cah. Biol. mar. 19: Belge, Expl. Parc Nat. Upemba, Mission G. F. de Witte, 21: 23-36. 1-62. Gremigni, V., 1979. An ultrastructural approach to planarian Meixner, J., 1928. Der Genitalapparaat der tricladen unde seine . Syst. Zool. 28: 345 355. Beziehungen zu ihrer allgemeinen Morphologie, Phylogenie, Holmquist, C. & Karling, T. G., 1972. Two new species of Okologie und Verbreitung. Zeitschr. Morph. Okol. Tiere. I 1: interstitial marine triclads from the North American Pacific 570 612. coast, with comments on evolutionary trendsand systematics Pielou, E. C., 1980. Biogeography. John Wiley & Sons, New in Tricladida (Turbellaria). Zool. Scr. 1: 157-184. York. pp. ix + 351. Hyman, L. H., 1944. Marine Turbellaria from the Atlantic coast Riedl, R., 1978. Order in Living Organisms. John Wiley &Sons, of North America. Am. Mus. Novit. 1266: 1-15. Chichester. pp. xii + 313. Karling, T. G., 1974. On the anatomy and affinities of the turbellarian orders. In: Eds. Riser, N. W. & Morse, M. P., The Biology of the Turbellaria. McGraw-Hill, New York, pp. 1-16.