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104. Booth, C.L., D.S. Woodruff and S.J. Gould. Lack of significant associations between allozyme heterozygosity and phenotypic traits in the land snail Cerion. Evolution 44(1):210-213. (1989g). RESEARCH ARTICLE A 104 EIIOI",itIft. ,,,,).'990. pp. 21G-213 LACK OF SIGNIFICANT ASSOCIATIONS BETWEEN ALLOZYME HETEROZYGOSITY AND PHENOTYPIC TRAITS IN THE LAND SNAIL CHRION CAREY L. BOOTH.' DAVID S. WOODRUFF. Dcpanmcn: of Ria/ot.!' & Crlllrr for Mo/rrll/or Gcnaics. UII;I'rrsil)' of California SOli Virgo. La Jolla, C., 92093 AND STEPHEN M,/sr,/m JAY GOULD of Comparative F.OO/O[:.!'.llarvard UII;I·rrS;I)'. Cambridge, MA 02 138 Received April 17. 1989. The: regulation and significanc:c: of phenotypic variation remain central problems at the interface of molecular genetics with classical morphology and evolutionary ecology. Hence. the rel:llion~hip between genotype and phenotype: is of great interest to evolutionary biologists. and over the laM 15 ye:lrs. m:lny reports of :llIo/.)'me-heter07Yllute I"henntYl"ic ~upcri. ority have been published :lnd reviewed (MiIlOIl and Grant, 1984; Allendorf and Leary, I 9li6; Zouru~ and FoJt7~ 1987), Individuals hC'tC'roJ:ygous at some locus lire often larger. faster growing, longer-lived, metabolically more efficient, or more fecund than individuals homozygous at that locus. Similarly. individuals with more heterozygous loci arc often superior to individuals with fewer heterozygous loci, and in some popu- , Present address: Department lege, Portland. OR 97202, of Biologv, Reed Col- Accepted October 13. 1989 lalions. the frcqut'nC")' of ht'Icro7~'!ol"$ increases with cohort age. Heterozygosity is also on en pcsitivcly associated with developmental homeostasis: individuals with more h('t('rO/YltoIlS loci may exhibit less phenotypic variability than individuals with fewer heiero7ygouS loci. However. there arc reports in which no rel:"ion~hip was found between h('tero/n!O~ity and f". m'ss correlates rnr some loci (Koehn ct al .. I 'IR!!) and even some reports of hOI1l01YllOIC:5ullCriorily (Allendorf and Leary, 19Rfl). In this note. we report mainly a lack of signiflC'ant associations ofheter07.ygosit)· with phC'notypic traits and variation in Cerion land snails. Mechanisms underlying positive relationships between allczyrnc h('tero1ygosity and fitness correlates in any given case are usually unknown. Some possible mechanisms are dominance or ovcrderninance either at the loci examined or at other loci that arc in linkage disequilibrium with the studied loci (Millon and Grant. 1984; Smouse. 1986; Zouros and Foltz, 1987). Under 211 NOTES AND COMMENTS the dominance hypothesis, heterozygosity serves to cover deleterious recessives. The overdorninancc hypothesis implies that heterozygous genotypes arc bcucr per se (Smouse, 1986). At a given locus, thc hetcrozygote will outperform the homozygmcs. Heterosis is the reverse of inbreeding depression and can be the result of either increased heterozygosity at a large number of overdominant loci or decreased expression of a small number of deleterious recessive alleles (Millon and Grant, 1984), With associative overdorninance, the studied loci are not directly affecting the traits, but they are in linkage disequilibrium with loci that do (Zouros and Foltz, 1987). Individuals heterozygous at the studied loci are more likely to be heterozygous at other loci which may have deleterious recessives; therefore, heterozygotes will have higher fitness than homozygotes (Nei, 1987). In this study, we analyzed the relationships between an individual's multilocus heterozygosity and measures of the same individual's shell morphology in West Indian land snails (O'r;oll bellda/h). We sought assoelations between heterozygosity and measures of both shell morphology and phenotypic variability. Cerion arc well suited to studies of phenotypic variation, as their shells bear a complete record of their ontogeny (Woodruff, 1978). A recurved lip marks the cessation of shell growth in adults, and as the protoconch is retained, size and shape at different ontogenetic stages can be measured. More generally, Cerion are especially interesting as subjects for studies of phenotypic diversity, as their shells exhibit extremely high interpopulation variability in size, shape, sculpture (ribbing), and coloration. Such diversity led to the recognition of more than 600 species, whose validity and evolutionary relationships are now under critical review (Gould and Woodruff, 1986, 1987; Woodruff and Gould, 1980, 1987), MATERtALS AND METHODS Gould and Woodruff'( 1978) collected and published the data used for this analysis, and only a brief overview of the methods is repeated here, The morphological and genetic data were originally used to discriminate among two subspecies and their hybrids, which occur on the islands of Lillie Bahama Bank. The subset for C. bendalli was used for this analysis, Adult shells are elongate or pupilliform, typically 24-30 mrn long, and have 7-9 whorls. Twenty adult snails were collected in the smallest possible area (typically 1m2) around a randomly chosen point at each of I 3 different sites. Each individual's shell was measured for 16 continuous characters and three meristic characters defined in Gould et al. (1974) and Gould and Woodruff (1978). Here we used only the nine continuous and two meristic characters that had greatest repeatability of measurement (K. M. Ligarc's [unpubl.] results discussed in Gould and Woodruff] 1986J; Table I). Starch-gel electrophoresis of each individual's foot muscle revealed 20 interpretable loci. Of thc corrcsponding enzymes, six were found to be polymorphic: esterase-Z, malate dehydrogenase- I, malate dchydrogcnasc-Z, 6-phosphogluconate dehydrogenase- I, asparuue aminotransferase (formerly called glutamic oxalacetate transaminase), and leucine aminopeptidase, Each individual was heterozygous at 0-5 loci; no individual was heterozygous at all six 10C'i,We used the number of heterozygous loci per individual (h), without regard for locus or genotype, as our measure of hetcrozygosity, following Zouros and Foltz (1987). We did statistical analyses using Stat View and SYS· TAT software for the Macintosh microcomputer. Snails were categorized into four heterozygosity classes: h 0, I, 2, and z 3; sample sizes of each class were as follows: N(h .. 0) - 53, N(h ~ I) = 81, N(h ~ 2) - 82, N(h 2: 3) .. 44. The ipdividuals with three, four, or five heterozygous loci were placed into one class due to the small number of individuals with four (N - 10) or five (N - I) heterozygous loci, A principal-components analysis reduced the nine continuous characters to three axes, which explained 94.6% of the total variance. Correlations were calculated to assess the relationship. if any, between the mean scores for the first three axes and the heterozygosity classes, between the I I characters and the heterozygosity classes, and among the characters that showed a significant correlation with the heterozygosity classes. The sequential Bonferroni method was used to determine the significance level for each column of tests (Rice, 1989). To compare phenotypic variability among the heterozygosity classes, we used Levene's test which is robust to deviations from normality (Schultz, 1983), The median phenotype: value for each heterozygosity class was subtracted from each phenotype: value in that class, and the absolute values of these differences were calculated. Correlations between the differences from the median and the heterozygosity classes were calculated. RESULTS The first axis of the principal-components analysis explained 85.0%, the second axis explained 6,7%, and the third axis explained 2,9% ofthc total variance. Shell length and aperture height loaded most strongly on the first axis, which was expected, as first axes are usually size axes for biological measurements of this type. Aperture width and width at the fourth whorl loaded most strongly on the second axis, There was no significant correlation between the individuals' axis scores and the heterozygosity classes for the first, second, or third axes. The advantage of using a principal-components analysis is that several variables can be tested simultaneously, thus avoiding the problem of multiple statistical tests. As there were no significant correlations between the axis scores and heterozygosity, the individual traits were also tested, and the sequential 13onferroni method was used to adjust the cxperimentwise significance level, The numberofribs on the fourth and sixth whorls were thc only two traits for which a significant correlation was found with the heterozygosity classes (Table I). These two traits were also significantly positively correlated with each other (r = 0.74, P < 0,000 I), and the number of ribs on the fourth whorl was significantly negatively correlated with shell width (r - -0,37, P < 0.000 I). Levene's test for average deviations from the median revealed no significant correlation between deviations from the median for any trait and the heterozygosity classes (Table I), DISCUSSION This study meets at least four ofZouros' (1987) five conditions that favor detection ofa positive correlation between heterozygosity and phenotype. The degree of 212 NOTES AND COMMENTS TABLEI. Correlation coefficients (r) between trait values and hctcrozygoslty-ctasscs and between trait deviations from the medians and hcterolygosity.classcs of Cerion bcndalli. Cllml.. "'"I1( Contlalion or .rail ,nil dt'"..iation Trail Shell length Shell width Protoconch width Height to whorl 4 Whorl-4 width Weight Whorl number Aperture width Aperture height Number ofwhorl-4 ribs Number of whorl-S ribs wilh he-1frolYlosily wnh ht"lrro')"('ISIIy 0.Q7 0.10 -O.QJ -0,06 -0.02 -0,05 0.09 -0,01 -0,04 -0,27-0,28- .,. < 0.004' lllIe no..(~""IIili,II;("'_,," kvd • 0.0"" lOr each column). -0.10 0.04 0.08 0.13 0.04 0.01 0.06 -O.QJ -0,12 0,00 O.QJ • 0.004' would be expected between trait variance and heterozygosity, The negative assoclation could be simply due to the fact that there arc more homozygote classes than heterozygote classes. In contrast to the above exeeetations. we found no relationship ror II traits. The absence of associations may indicate that the traits arc not afl'ccted by the loci studied, that the loci studied arc not indicative or the level of heterozygosity of the entire genome (Chakraborty and Ryman, 1983), or that heter07.ygosity and developmental homeostasis are not always related, In conclusion, we mainly found a lack orassociation between multilocus hetero7.ylto~ity and various measures or phenotype and phenotypic variance, We believe it is important to report the instances in which no significant relationship was found, as well as those few positive and negative associations. It seems that past researchers have overemphasized the few strong associations at the expense of the message conveyed by the majority or cases in which there is none, Biased reporting or only positive results can severely distort our view of reality (Begg and Berlin, 1988), ACKNOWLEDGMENTS We thank I, Beardmore and T, D. Price: for helpful conversations. Thc commems ofn. D. Collier, and our reviewers were also very uscful, We thank an anonymous reviewer ror the suggestion to consider the efl'ccts of pooling the data rrom the 13 sites, This research was supported, in part, by NSF grants DEB 7714618 and 8207540 (to D,S,W, and 5,J,O,) and-BSR-SSOO733 (to D.S, W,) and NSF and US PHS prc:doctoral fellowships (to C.LIJ,), hetcrozygosity was measured for a large numhcr ofloci (20, of which sill were polymorphic); the phenotypic traits studied are likely to be afl'eeted by a largc number or loci; nongenetie factors likely to afl'ect these: characters are probably random; and the sample size of 260 is large and representative of the_aene pool The Jifth condition (steady-state linkage disequilibrium) has not yet been assessed in Cerion. We found that only two of the I I traits examined were significantly correlated with the hetcr07ygo~ity LITERATURE CmD classes, Because these two traits were correlated with ALLENDORF,F, W.. ANDR, F, LEARY. 1986, Heteroeach other, there was actually only one relationship 7ygosity and fitness in natural populations of aniwith heterozygosity, The significance, if any, of a demals, pp. 57-76, In M, E. Soule (ed.), Conservation crease: in the number of ribs on the fourth and sixth Biology, Thc Sciencc orScareity and Diversity, Sinwhorls with an increase in heler07.),Sosit)' is unknown, aucr, Sundcrland, MA, The ribbing traits were suspected or being an adaptaBEOO,C, B., AND J, A, DERLtN, 1988, Publication tion associated with defense: from crushing predators; bias: A problem in intcrpreting medical data, J, however, J, Quenson (reported in Oould and WoodrulT Roy, Slat. Soc, A 151:419-463, (1978) found that shell size (weight and height) was CHAKRABORTY, R" ANDN. RYMAN, 1983, Relationmore important than ribbing in determining shell ship of mcan and variance of scnotypie values with strength, Some workers have found allozymc-phenobeterozygosiry per individual in a natural populatype covariation at some loci but not at othcrs (Koehn tion. Genetics 103:149-152, et aI., 1988; Pemberton et aI., 1988), so analyses based GOULD,S. J .. AND D, S, WOODRUFF, 1978, Natural on multiloeus hetero7.ygosity such as ours may miss history of Cerion VIII: Little Bahama lJank-A resome single-locus eflects. vision based on genetics, morphometries, and geoIn pooling the 13 sites, there was a risk of obscuring graphic distribution. Dull. Mus, Compo Zool. 148: a significant correlation between heterozygosity and 371-415, phenotype or or finding ~ignifleant correlations where --. 19R6, Evolution and svstematics of Ccrion there were none within the sites. In examining the dis(Mollusca: Pulmonata) on Ne~ Providence Island: tribution of individuals in different heter07.ygosityA radical revision, Bull, Amer. Mus, Nat, Hist. 182: classes in the 13 sites, snails in five sites were found 389-490. to have relatively high hetcro~ygosity, and snails in --, 1987. Systematics and levels of covariarion eight sites were found to have lower heterozygosiry. in Cerion from the Turks and Caieos islands, Bull After pooling the high-hcterozygosity sites in one group Mus, Comp. Zool, 151:321-363, and the low-heterozygosity sites in another group and GOULD, S, J.. D, S. WOODRUFF,ANDJ, P, MARTIN, redoing the correlation analyses, no significant corre1974, Gcnetics and morphometries of Cerion at lation was found for either group for any of the I I Pongo carpet: A new systematic: approach to this traits. cnigmatie land snail, S)·5t. Zool, 2.1:5IR-535, Lerner ( I954) reviewed evidence that developmental KOEIIN,R, K., W, J, DIEHL.ANDT, M. ScOTT. 1988. homeostasis is greater in individuals with more hctThe differential contribution by individual enerozygous loci and, thus, that a negative rclntionship zyrncs of glycolysi5 and I'rotein C':lIaboli~m to the 213 NOTES AND COMMENTS relationship between heterozygosity and growth rate in the: coot clam, Mulinia lateralis. Generics I 18: 121-130. LERNER,I. M. 1954. Genetic Homeostasis. Oliver & Boyd, Edinburgh, U,K, MITTON,J. B" ANDM. C. GRANT. 1984. Associations among protein heterozygosity, growth rate, and developmental homeostasis. Ann. Rev. Ecol. Syst. 15: 479-499, NEI, M. 1987. Molecular Evolutionary Genetics. Columbia Univ. Press, N.Y. PEMBERTON, J. M., S. D. ALBON,F. E. GUINNESS,T, H. CWTTON-BROCK,ANDR. J. BERRY. 1988. Genetic variation and juvenile survival in red deer, Evolution 42:921-934. RICE,W. R, 1989, Analyzing tables of statistical tests. Evolution 43:223-225. SCHULTZ,B. 1983. On Levene's test and other statistics of variation. Evol. Theor. 6: 197-203. SMOUSE,P. E. 1986. The fitness consequences of'muliiple-locus heterozygosity under the multiplicative overdominance and inbreeding depression models. Evolution 40:946-957. WOODRUFF,D. S. 1978. Evolution and adaptive ra- diation of Cerion, a remarkably diverse group of West Indian land snails. Malacologia 17:223-239, WOODRUFF,D. S., ANDS. J. GOULD. 1980. Geographic differentiation and speciation in Cerion: A preliminary discussion of patterns and processes, BioI. J. Linn. Soc. 14:389-416. ---. 1987. Fifty years of interspecific hybridization: Genetics and morphometries of a controlled experiment involving the land snail Cerion in the Florida Keys. Evolution 41:1022-1045. ZoUROS, E. 1987, On the relationship between heterozygosity and heterosis: An evaluation of the evidence from marine mollusks, pp. 255-270. In M. C. Rattazi, J. G. Scandalios, and G. S. Whitt (eds.), Isozyrnes: Current Topics in Biological and Medical Research, Vol. 15, Liss, N.Y. ZoUROS,E., ANDD. W. FOLTZ, 1987, The use of allelic isozyme variation for the study of heterosis, pp. 159. In M. C. Rauazi, J. G. Scandalios, and G. S. Whitt (eds.), Isozymes: Current Topics in Biological and Medical Research, Vol. 13. Liss, N.Y, Corresponding Editor: R. C. Vrijenhoek