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Genetic evidence for the occurrence of a cryptic species with the littoral nemerteans Lineus ruber and L. viridis (Nemertea: Anopla)

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Abstract

Lineus ruber and L. viridis are common intertidal heteronemerteans found on the coasts of northern Europe and the east coast of North America. The two species resemble each other morphologically and were synonymised for many years prior to being separated on the basis of larval development. In this study, specimens of L. ruber and L. viridis were collected from sites along the west and southwest coast of Britain, northern France and the east coast of North America. The external morphology and allele frequencies of isozymes of the two species were compared from all sites. The external morphology of L. ruber and L. viridis was similar but they could generally be separated by colour. Allele frequencies for up to 13 enzyme loci between sympatric populations of L. ruber and L. viridis indicated that these two species are genetically very different (Nei's genetic identity=0.090 to 0.083). Allele-frequency data also indicated the presence of a third genetic type occurring sympatrically with populations of both L. ruber and L. viridis on the coasts of Britain and France but not on the coast of North America. Fixed differences in allele frequencies between populations of the third genetic type and sympatric populations of L. ruber and L. viridis were observed across multiple loci. Genetic identity between the third genetic type and sympatric populations of L. ruber and L. viridis were extremely low (Nei's genetic identity =<0.078). Such large genetic differences between populations indicate a barrier to gene flow and reproductive isolation. The aberrant type, which exhibits sufficient morphological variation to prevent individuals being distinguished from those of both L. ruber and L. viridis, therefore represents a separate species. The low genetic identities found in intrageneric comparisons of species found in this study have been found in other studies on nemerteans. They may indicate systematic problems within these groups or other phenomena such as morphological stasis.

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References

  • Arnold G (1898) Zur Entwicklungsgeschichte des Lineus gesserensis O.F. Müller (L. obscurus Barrois). Trudū imp S-peterb Obshch Estest 28:21–30

    Google Scholar 

  • Ayala FJ (1975) Genetic differentiation during the speciation process. In: Dobzhanskv T, Hecht MK, Steere WC (eds) Evolutionary biology Vol. 8. Plenum Press, New York, pp 1–78

    Google Scholar 

  • Ayala FJ (1983) Enzymes as taxonomic characters. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, pp 3–26

    Google Scholar 

  • Balakirev ES, Manchenko GP (1984) Vnutrividovaya geneticheskaya izmenchivost belkov u nemertinui Lineus torquatus. Genetika 20:2070–2071

    Google Scholar 

  • Barrois J (1877) Mémoire sur l'embryologie des Némertes. Annls Sci nat (sér Zool) 6 (No. 3):1–232

    Google Scholar 

  • Bierne J (1962) La régénération de la trompe ches les Némertes. Bull biol Fr Belg 96:481–504

    Google Scholar 

  • Bierne J (1964) Maturation sexuelle anticipée par décapitation de la femelle chez l'hétéronémerte Lineus ruber Müller. C r hebd Séanc Acad Sci, Paris 259:4841–4843

    Google Scholar 

  • Bierne J (1966) Localisation dans les ganglions cérébroïdes du centre régulateur de la maturation sexuelle chez la femelle de Lineus ruber Müller (Hétéronémertes). C r hebd Séanc Acad Sci, Paris 263:1572–1575

    Google Scholar 

  • Bierne J (1970a) Influence des facteurs hormonaux gonado-inhibiteur et androgène sur la differentiation sexuelle des parabionts hétérosexués chez un némertian. Année biol 9:395–400

    Google Scholar 

  • Bierne J (1970b) Recherches sur la différenciation sexuelle au cours de l'ontogenèse et de la régénération chez le némertien Lineus ruber (Müller). Annls Sci nat (sér Zool). 12:181–298

    Google Scholar 

  • Bierne J (1970c) Aspects expérimentaux de la différenciation sexuelle chez Lineus ruber (Hétéronémertes). Bull Soc zool Fr 95:529–543

    Google Scholar 

  • Bierne J (1979) Viable animals obtained by grafting pieces from several nemertean adults. Transplantation 29:74–75

    Google Scholar 

  • Bierne J (1983) Nemertina. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of the Invertebrates. Vol. 1. Oogenesis, oviposition and oosorption. John Wiley & Sons Ltd, London, pp 147–167

    Google Scholar 

  • Brunberg L (1964) On the nemertean fauna of Danish waters. Ophelia 1 (1):77–111

    Google Scholar 

  • Corrêa DD (1963) Nemerteans from Curaçao. Stud Fauna Curaçao 17:41–56

    Google Scholar 

  • Ferguson A (1980) Biochemical systematics and evolution. Blackie & Son, Glasgow

    Google Scholar 

  • Fisher FM, Cramer NM (1967) New observations on the feeding mechanism in Lineus ruber (Rhynchocoela). Biol Bull mar biol Lab, Woods Hole 132:p 464

    Google Scholar 

  • Fisher FM, Oaks JA (1978) Evidence for a nonintestinal nutritional mechanism in the rhynchocoelan, Lineus ruber. Biol Bull mar biol Lab, Woods Hole 154:213–225

    Google Scholar 

  • Fisher RA (1935) The logic of inductive inference. Jl R statist Soc 98:39–54

    Google Scholar 

  • Franzén Å (1983) Nemertina. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Vol. II Spermatogenesis and sperm function. John Wiley & Sons Ltd, London, pp 159–170

    Google Scholar 

  • Friedrich H (1935) Studien zur Morphologie, Systematik and Ökologie der Nemertinen der Kieler Bucht. Arch Naturgesch 4:293–375

    Google Scholar 

  • Gibson R (1982) British nemerteans. In: Kermack DM, Barnes RSK (eds) Synopses of the British fauna. Cambridge University Press, Cambridge, pp 1–212

    Google Scholar 

  • Gibson R (1995) Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution. J nat Hist (in press)

  • Gontcharoff M (1951) Biologie de la régénération et de la reproduction chez quelques Lineidae de France. Annls Sci nat (sér Zool) 13:149–235

    Google Scholar 

  • Gontcharoff M (1957) Étude des rhabdites de la trompe de Lineus ruber (némertien) au microscope électronique. C r hebd Séanc Acad Sci Paris 244:1539–1541

    Google Scholar 

  • Gontcharoff M (1960) Le développement post-embryonnaire et la croissance chez Lineus ruber et Lineus viridis (Némertes Lineidae). Annls Sci nat (sér Zool) 2:225–279

    Google Scholar 

  • Harris H, Hopkinson DA (1978; and subsequent supplements) Handbook of enzyme electrophoresis in human genetics. North Holland Publishing Co., Amsterdam

    Google Scholar 

  • Hubrecht AAW (1886) Contributions to the embryology of the Nemertea. Q Jl microsc Sci 26:417–448

    PubMed  Google Scholar 

  • Jennings JB (1962) A histochemical study of digestion and digestive enzymes in the rhychocoelan Lineus ruber (O.F. Müller) Biol Bull mar biol Lab, Woods Hole 136:405–433

    Google Scholar 

  • Jennings JB, Gibson R (1969) Observations on the nutrition of seven species of rhychocoelan worms. Biol Bull mar biol Lab, Woods Hole 136:405–433

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Lechenault H (1965) Neurosécrétion et osmorégulation chez les Lineidae (Hétéronémertes). C r hebd Séanc Acad Sci Paris 261:4868–4871

    Google Scholar 

  • Lessios HA (1992) Testing electrophoretic data for agreement with Hardy-Weinberg expectations. Mar Biol 112:517–523

    Google Scholar 

  • Ling EA (1969) The structure and function of the cephalic organ of the nemertine Lineus ruber. Tissue Cell 1:503–524

    Google Scholar 

  • Ling EA (1970) The structure and function of the cephalic organs of the nemertine (Lineus ruber and Amphiporus lactifloreus). Ph.D. thesis. University of Cambridge, Cambridge, UK

    Google Scholar 

  • Ling EA (1971) The proboscis apparatus of the nemertine Lineus ruber. Phil Trans R Soc (Ser B) 262:1–22

    Google Scholar 

  • Mayr E (1957) Species concepts and definitions, in the species problem. Publs Am Ass Advmt Sci 1–22

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, USA

    Google Scholar 

  • McDermott JJ, Roe P (1985) Food, feeding behaviour and feeding ecology of nemerteans. Am Zool 25:113–125

    Google Scholar 

  • Marphy RW, Sites JW, Buth DG, Haufler CH (1990) Proteins. I. Isozyme electrophoresis. In: Hillis DM, Moritz C (eds) Molecular systematic. Sinauer Associates, Inc. Sunderland, Mass, USA pp 45–126

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, Austin, Tex 89:583–590

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nevo E (1978) Genetic variation in natural populations: patterns and theory. Theor Popul Biol 13:121–177

    PubMed  Google Scholar 

  • Nevo E, Beiles A, Ben-Schlomo R (1984) The evolutionary significance of genetic diversity: ecological demographic and life-history correlates. In: Mani GS (ed) Evolutionary dynamics of genetic diversity. Springer-Verlag, Heidelberg, pp 13–212

    Google Scholar 

  • Nordhausen W (1988) Impact of the nemertean Lineus viridis on its polychaete prey on an intertidal sand flat. Hydrobiologia 156:39–46

    Google Scholar 

  • Nusbaum J, Oxner M (1910) Studien über die Regeneration der Nemertinen. I. Regeneration bei Lineus ruber (Müll). Arch EntwMech Org 30:74–132

    Google Scholar 

  • Nusbaum J, Oxner M (1911) Weitere Studien über die Regeneration der Nemertien. I. Regeneration bei Lineus ruber Müll. Arch EntwMech Org 32:349–396

    Google Scholar 

  • Nusbaum J, Oxner M (1913) Die Embryonalentwicklung des Lineus ruber Müll. Ein Beitrag zur Entwicklungsgeschichte der Nemertinen. Zwiss Zool 107:78–197

    Google Scholar 

  • Richardson BJ, Baverstock PM, Adams M (1986) Allozyme electrophoresis. Academic Press, Sydney

    Google Scholar 

  • Riser NP (1974) Nemertinae. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Vol. 1. Acoelomate and pseudocoelomate metazoans. Academic Press, New York and London, pp 359–389

    Google Scholar 

  • Rogers AD (1993) Aspects of the genetics and taxonomy of marine nemerteans. Ph.D. thesis. University of Liverpool

  • Rogers AD, Junoy J, Gibson R, Thorpe JP (1993) Enzyme electrophoresis, genetic identity and description of a new genus and species of heteronemertean (Nemertea, Anopla) from northwestern Spain and North Wales. Hydrobiologia 266:219–238

    PubMed  Google Scholar 

  • Schmidt GA (1934) Ein zweiter Entwicklungstypus von Lineus gesserensis-ruber O.F. Müller. (Nemertini). Zool Jber Neapel 58:607–660

    Google Scholar 

  • Schmidt GA (1946) Genetic and ecological relations of littoral nemerteans of the genus Lineus. Dokl Acad Nauk SSSR 51:405–407

    Google Scholar 

  • Scozzani R, Ulizzi A, Ferracin A, Lunadei M (1980) An electrophoretic polymorphism in Triturus cristatus carnifex (Amphibia, Urodela). Experientia 36:p 645

    PubMed  Google Scholar 

  • Selander RK (1977) Genic variation in natural populations. In: Ayala FJ (ed) Molecular evolution. Sinauer Associates Incorporated, Sunderland, Mass, pp 21–45

    Google Scholar 

  • Solé-Cava AM, Boury-Esnault N, Vacelet J, Thorpe JP (1992) Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea. Mar Biol 113:299–304

    Google Scholar 

  • Solé-Cava AM, Klautau M, Boury-Esnault N, Borojecic R, Thorpe JP (1991) Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Mar Biol 111:381–386

    Google Scholar 

  • Solé-Cava AM, Thorpe JP (1990) High levels of genetic variation in marine sponges. In: Rutzler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, pp 332–337

    Google Scholar 

  • Solé-Cava AM, Thorpe JP (1991) High levels of genetic variation in natural populations of marine lower invertebrates. Biol J Linn Soc 44:65–80

    Google Scholar 

  • Solé-Cava AM, Thorpe JP, Kaye JG (1985) Reproductive isolation with little genetic divergence between Urticina (=Tealia) felina and U. eques (Anthozoa: Actiniaria). Mar Biol 85:279–284

    Google Scholar 

  • Sundberg P, Janson K (1988) Polymorphism in Oerstedia dorsalis (Abilgaard, 1806) revisited. Electrophoretic evidence for a species complex. Hydrobiologia 156:93–98

    Google Scholar 

  • Swofford DL, Selander RB (1989) Biosys-1. A computer program for the analysis of allelic variation in population genetics and biochemical systematics. Release 1.7. Illinois Natural History Survey, Champaign, Illinois

    Google Scholar 

  • Thiel M, Reise K (1993) Interaction of nemertines and their prey on tidal flats. Neth J Sea Res 31:163–172

    Article  Google Scholar 

  • Thorpe JP (1982) The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. A Rev Ecol Syst 13:139–168

    Article  Google Scholar 

  • Thorpe JP (1983) Enzyme variation, genetic distance and evolutionary divergence in relation to levels of taxonomic separation. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London pp 131–152

    Google Scholar 

  • Thorpe JP, Solé-Cava A (1994) The use of allozyme electrophoresis in invertebrate systematics. Zoologica Scr 23:3–18

    Google Scholar 

  • Vernet G (1966) Les pigments de Lineus ruber (O.F. Müller) (Hétéronémertes Lineidae). C r hebd Séanc Acad Sci Paris 263:191–194

    Google Scholar 

  • Vernet G (1970) Ultrastructure des photorécepteurs de Lineus ruber (O.F. Müller) (Hétéronémertes Lineidae). I. Ultrastructure de I'oeil normal. Z. Zellforsch mikrosk Anat 104:494–506

    PubMed  Google Scholar 

  • Vernet G (1992) Localisation du réflexe lucifuge dans les ganglions cérébroïdes dorsaux de la némerte marine, Lineus ruber (O.F. Müller): étude expérimentale. Can J Zool 70:750–752

    Google Scholar 

  • Vernet G, Bierne J (1993) The influence of light and sea water temperature on the reproductive cycle of Lineus ruber (Heterone-mertea). Hydrobiologia 266:267–271

    Google Scholar 

  • Ward RD, Beardmore JA (1977) Protein variation in the plaice (Pleuronectes platessa). Genet Res 30:45–62

    PubMed  Google Scholar 

  • Wake DB, Roth G, Wake MH (1983) On the problem of stasis in organismal evolution. J theor Biol 101:211–224

    Google Scholar 

  • Williams KA, Skibinski DOF, Gibson R (1983) Isoenzyme differences between three closely related species of Lineus (Heteronemertea). J exp mar Biol Ecol 66:207–211

    Article  Google Scholar 

  • Willmer EN (1970) Cytology and evolution. 2nd ed. Academic Press, New York and London

    Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395–420

    Google Scholar 

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Communicated by J. Mauchline, Oban

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Rogers, A.D., Thorpe, J.P. & Gibson, R. Genetic evidence for the occurrence of a cryptic species with the littoral nemerteans Lineus ruber and L. viridis (Nemertea: Anopla). Marine Biology 122, 305–316 (1995). https://doi.org/10.1007/BF00348944

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