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Population genetics of Melampus bidentatus (Gastropoda: Pulmonata): the effect of planktonic development on gene flow S. W. Schaeffer 1, E. C. Kellerl, Jr. & N. E. Buroker2 i Dept. of Biology, West Virginia University, Morgantown, WV26506, USA 2 Center for Environmental and Estuarine Studies, University of Maryland, Crisfield, Md, USA Abstract Melampus bidentatus has restricted gene flow of gametes and the potential for extensive gene flow of their planktonic larvae. We used genetic data to examine the influence of these opposing forces on the population structure of six Delmarva Peninsular populations. We analyzed the population structure of these six populations using twenty-three electrophoretic loci. Two ocean populations gave the appearance of large panmictic populations, while the other four populations appeared to be highly subdivided due to either restricted gene flow or age-structuring of the population. Two distinct groups of populations are apparent, which accounts for the extreme interpopulation heterogeneity. These data suggest that the direction of tides and currents limit the effectiveness of the planktonic dispersal stage of M. bidentatus in overcoming restricted gene flow of gametes. Introduction out into the offshore plankton layer with the ebbing tide. The larvae spend two weeks developing into Successful gene flow requires dispersal of gam- adults in the plankton layer. Following planktonic etes or newly formed zygotes to a new popu- development, the adults settle into the salt marsh lation and subsequent establishment of these gam- where they reside for their remaining two to three etes or zygotes (Endler, 1977; Scheltema, 1975). years of life (Russell-Hunter et al., 1972). McCracken & Bussard (1981) showed that re- The terrestrial existence of M. bidentatus should stricted gene flow in terrestrial snails increased the increase genetic differences between populations, genetic differences between populations. Other but a planktonic larval stage has the potential to sedentary organisms show similar patterns (Levin & reduce these genetic differences. In this paper we Kerster, 1974; Schaal, 1975; Workman & Nis- examine the influence of these two opposing forces wander, 1970). On the other hand, extensive gene on the population structure of natural populations flow in marine invertebrates reduces genetic differ- of M. bidentatus. ences between populations (Buroker et al., 1979; Koehn et al.. 1976). These experimental results are Material and methods consistent with Wright's (1943) isolation-by-dis- tance model. We sampled six natural populations ofM. biden- Melampus bidentatus (Say) is a pulmonate snail tatus located on the peninsula formed by Delaware, which lives above the average high-tide mark of Maryland and Virginia (Delmarva Peninsula). coastal and estuarine salt marshes along the Atlan- Three Atlantic Ocean localities (Fenwick Island, tic Ocean and Gulf of Mexico (Holle & Dineen, Delaware; Wallops Island, Virginia; and Cape 1957). Hatching M. bidentatus larvae are washed Charles, Virginia) and three Chesapeake Bay sites Genetica 66, 223-229 (1985). © Dr W. Junk Publishers, Dordrecht. Printed in the Netherlands. 224 phoglucose isomerase (pgi), phosphoglucomutase ~,. Surfacel~ .--P7" Current I'-k,~ .... -~ y" (pgm), and superoxide dismutase (sod). The no- menclature of Ayala et aL (1972) was used to de- scribe our electrophoretic loci. "'Current I I k N We calculated allele frequencies for each poly- morphic locus in each population. A locus was considered polymorphic if the frequency of the most common allele in any of the six populations sampled was less than or equal to 0.95. An analysis of population structure compares the observed gene and genotypic frequencies with those expected under the assumption of random mating. Depar- tures from random mating suggest that selection, inbreeding or other evolutionary forces are acting I ..... on the individuals of the population. We tested departures of genotypic frequencies from the ex- pected proportions under random mating by means of chi-squared tests for goodness-of-fit. A chi- Chesapeake - f squared test for homogeneity or gene frequency was B j, c v , ,/. Y. ' . used to detect departures from random mating be- \ tween populations (Schaal, 1975; Workman & Nis- wander, 1970). Genetic similarities and genetic dis- tances for all pairwise comparisons were calculated using Nei's (1972) formulas. We clustered Nei's ccV# / genetic distances using the UPGMA algorithm of Sheath & Sokal (1973). Results The six populations were monomorphic for the Fig. 1. A map of the Delmarva Peninsula showing the six Me- same electrophoretic allele at thirteen enzyme loci lampus bidentatus sampling sites. The map also shows the cur- of the twenty-three loci scored for M. bidentatus. rents along the Atlantic coast and in the Chesapeake Bay (after Scheletema, 1975). The six populations are: Fenwick Island Ten loci examined were polymorphic and in some (FI), Wallops Island (Wl), Cape Charles (CC), Eastville (EV), cases highly so with six electromorphs or more. The Cashville (CV), and Crisfield (CF). polymorphic loci were: acp-2, ald, ap, est-2, idh, !ap-1, lap-2, lap-3, 6-pgd, and sod. Our estimate of (Eastville, Virginia; Cashville, Virginia; and Cris- percent polymorphic loci, P = 0.435 + 0.073, was field, Maryland) were selected (Fig. 1). We col- within the range observed for other marine and lected 125 snails from each population and stored land snails (Nevo, 1978; Selander, 1976). The aver- them at -20 o C for electrophoresis. Salinity meas- age individual heterozygosity, H = 0.196 + 0.005, urements were taken at each site. Table 1. Average salinity ± standard error for six Delmarva Fourteen enzyme systems involving 23 loci were Peninsular sampling sites. Salinity is given in parts per thousand. examined using horizontal starch gel electrophore- sis (see Schaeffer, 1980). We stained for the follow- Population Salinity ± SE ing enzymes: acid phosphatase (acp), aldolase (aid), Fenwick Island 26.0 + 2.5 aminopeptidase (ap), aspartate aminotransferase Wallops Island 36.9 + 4.3 (aat), esterase (est), isocitrate dehydrogenase (idh), Cape Charles 31.7 + 6.0 leucine aminopeptidase (lap), malate dehydrogen- Eastville 20.6 ± 1.3 Cashville 19.4 + 1.5 ase (mdh), malic enzyme (me), muscle protein (rap), Crisfield 18.3 ± 3.5 6-phosphogluconate dehydrogenase (6-pgd), phos- 225 was greater than that reported in land or marine ville, Cashville, and Crisfield populations. These snails. Salinities for each site are given in Table !. populations had a deficiency of heterozygotes at We observed significant departures of our ob- most polymorphic loci. The other two populations, served genotypic frequencies from those expected Wallops Island and Cape Charles, exhibited few under random mating in the Fenwick Island, East- significant departures (Table 2). Table 2. Gene frequencies, number of alleles (N), relative mobilities (R M), observed heterozygosity (HO), and expected heterozygosity (HE) for six Delmarva Peninsular populations of Melampus bidentatus. Locus RM FI WI CC EV CV CF a~H-2 N 250*** 250 248 246*** 248 250 100 0.120 0.976 0.952 0.439 0.040 0.028 85 0.880 0.024 0.048 0.561 0.960 0.972 HO 0.016 0.048 0.097 0.016 0.048 0.056 HE 0.211 0.047 0.092 0.493 0.077 0.054 aM N 248 250 246 248 248 250*** 100 0.956 1.000 1.000 0.130 0.024 0.120 98 0.044 0.870 0.976 0.876 96 0.004 HO 0.056 0.195 0.056 0.136 HE 0.085 0.226 0.047 0.218 ap N 250*** 248 250 246*** 248 250*** 108 0,020 0.004 0.008 104 0.056 0.081 0.084 0.020 0.008 I00 0.132 0.746 0.680 0.183 0.004 96 0.772 0.161 0.200 0.138 0.032 0.016 92 0.020 0.008 0.024 0.114 0.109 0.084 88 0.004 0.455 0.802 0.856 84 0.073 0.044 0.028 80 0.004 0.016 78 0.012 HO 0.240 0.403 0.440 0.480 0.315 0.184 HE 0.383 0.411 0.490 0.721 0.341 0.259 est-2 N 248*** 248 244 246*** 248*** 250 109 0.020 0.024 0.073 0.053 107 0.012 0.125 0.115 0.053 0.016 0.004 105 0.024 0.246 0.139 0.053 103 0.036 0.218 0.152 0.061 0.065 0.044 102 0.036 0.069 0.119 0.049 100 0.032 0.238 0.217 0.045 0.028 98 0.024 0.048 0.078 0.118 0.085 0.076 97 0.060 0.016 0.045 0.045 96 0.016 95 0.141 0.016 0.020 0.045 0.351 0.088 93 0.185 0.025 0.159 0.073 0.244 91 0.153 0.008 0.102 0.113 0.228 89 0.052 0.077 0.016 0.024 87 0.125 0.004 0.098 0.129 0.212 85 0.057 0.024 0.008 0.044 83 0.028 0.004 0.016 0.089 0.028 79 0.012 0.004 0.012 0.008 HO 0.806 0.669 0.828 0.846 0.661 0.816 HE 0.891 0.812 0.868 0.914 0.821 0.825 idh N 248*** 250 250 244*** 244* 250 102 0.004 0.008 0.004 0.028 100 0.855 1.000 1.000 0.873 0.902 0.772 98 0.137 0.115 0.094 0.200 226 Table 2. Continued. Locus RM FI Wl CC EV CV CF 96 0,004 0.004 HO 0.153 0.057 0.148 0.280 HE 0.025 0.225 0.178 0.363 lap-I N 240 - 230 232 214"** 244*** 102 0.146 0.135 0.177 0.098 0.123 100 0.604 0.683 0.603 0.505 0,594 98 0.250 0.182 0.220 0,397 0.283 HO 0.525 0.461 0.526 0,449 0.533 HE 0.551 0.481 0.556 0.578 0.552 lap-2 N 248 224 246* 246*** 248*** 250 112 0.044 0.037 0.028 0.032 I10 0.331 0.138 0.254 0.192 108 0.423 0.289 0.544 0.644 106 0.109 0.085 0,149 0.112 104 0.032 0.054 0.069 0.130 0.020 0,020 102 0.028 0.295 0.256 0,110 0,004 100 0.016 0.527 0.463 0.126 98 0.016 0.103 0.167 0.073 96 0.022 0,045 0.012 HO 0,766 0.580 0,545 0.797 0.694 0.488 HE 0.695 0.621 0.685 0.838 0.616 0.534 lap-3 N 246*** 200 246 240*** 246*** 248 104 0.025 0.057 0.029 102 0.160 0,203 0.150 100 0.705 0.480 0.254 98 0.090 0.195 0.071 96 0.069 0.015 0.065 0.133 0.089 0,065 94 0.191 0,005 0.300 0.211 0.161 92 0,268 0.050 0.394 0.657 90 0.362 0,012 0.293 0.113 88 0.110 0.012
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    THE BIOLOGY OF TERRESTRIAL MOLLUSCS This Page Intentionally Left Blank THE BIOLOGY OF TERRESTRIAL MOLLUSCS Edited by G.M. Barker Landcare Research Hamilton New Zealand CABI Publishing CABI Publishing is a division of CAB International CABI Publishing CABI Publishing CAB International 10 E 40th Street Wallingford Suite 3203 Oxon OX10 8DE New York, NY 10016 UK USA Tel: +44 (0)1491 832111 Tel: +1 212 481 7018 Fax: +44 (0)1491 833508 Fax: +1 212 686 7993 Email: [email protected] Email: [email protected] © CAB International 2001. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data The biology of terrestrial molluscs/edited by G.M. Barker. p. cm. Includes bibliographical references. ISBN 0-85199-318-4 (alk. paper) 1. Mollusks. I. Barker, G.M. QL407 .B56 2001 594--dc21 00-065708 ISBN 0 85199 318 4 Typeset by AMA DataSet Ltd, UK. Printed and bound in the UK by Cromwell Press, Trowbridge. Contents Contents Contents Contributors vii Preface ix Acronyms xi 1 Gastropods on Land: Phylogeny, Diversity and Adaptive Morphology 1 G.M. Barker 2 Body Wall: Form and Function 147 D.L. Luchtel and I. Deyrup-Olsen 3 Sensory Organs and the Nervous System 179 R. Chase 4 Radular Structure and Function 213 U. Mackenstedt and K. Märkel 5 Structure and Function of the Digestive System in Stylommatophora 237 V.K.
  • Early Life-History of Melampus and the Significance of Semilunar Synchrony'

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    Reference : Biol. Bull., 143 : 623—656. ( December, 1972) EARLY LIFE-HISTORY OF MELAMPUS AND THE SIGNIFICANCE OF SEMILUNAR SYNCHRONY' W. D. RUSSELL-HUNTER, MARTYN L. APLEY AND R. DOUGLAS HUNTER2 I)epartment of Biology, Syracuse University, Syracuse, New lork 13210; Depart@nent of Biology, Brooklyn College, Brooklyn, New York 11210; and timeMarine Biological Laboratory, tl7oods Hole, ZlIassacI,iisetts 02543 Living in the higher levels of salt nuarshues, pulnuomuate snails of the genus Melampus are truly “¿amphibious.― In their respiration, they are land snails breathing air through pneumostome and lung. In their reproductiomu, they are primitive marine snails spawning large numbers of small eggs which yield plank tomiic veliger larvae on hatching. As adumbrated in earlier publications on flue biology of Melampu.s bidentatus (Russell Hunter and Apley, 1966 ; Apley, Russell Flunter and Avohizi, 1967 ; Apley, 1970 ; Russell-Hunter, Apley and Hunter, 1970), there is a significant temporal “¿fitting―of the reproductive events including egg laying and hatching to the two-week periodicity of spring tides. The sequence and “¿control―of these events and, in addition, of those of vehiger scttlement, metamorphosis and spat growth have now been examined in greater detail and flue more significant observations are reported in this paper. Minor parts of this account are derived from observations in the summers of 1964 and 1966, but most of the detailed observations on sequential “¿timing,―the experiments on “¿controls―and the observations on laval and spat growth, settlement amid meta nuorphosis were made and integrated during the sumnuer of 1970 at Woods Hole.