The Journal of Heredity 2001:92(6)
© 2001 The American Genetic Association 92:521-525
Brief Communication |
Inheritance of the General Shell Color in the Scallop Argopecten purpuratus (Bivalvia: Pectinidae)
From the Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Casilla 117, Coquimbo, Chile (Winkler and Estévez), Servicios y Equipos Marinos Ltda., Don Carlos 3187, Of. B, Las Condes, Santiago, Chile (Jollán), and Instituto de Fomentos Pesquero (IFOP), Doctor Marín 340, Coquimbo, Chile (Garrido).
Address correspondence to F. M. Winkler at the address above or e-mail: fwinkler{at}ucn.cl.
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Abstract |
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Although some external coloration and pigmentation patterns in molluscan shells may be attributable to environmental factors, most variation in these phenotypic characters depends on uncomplicated genetic mechanisms. Genetic research on inheritance of color variations in the north-Chilean scallop (Argopecten purpuratus) has now been expanded to analyze color segregation in juvenile scallops produced under controlled conditions employing self- and cross-fertilization. Calculations from the results were used for comparison with different numerical models based on Mendelian inheritance, and results were also obtained on the inheritance of a dorsoventral white line often observed on the left (upper) valve in this species. The results confirmed the hereditary basis for color variation in the shell of this scallop, suggesting a simple, dominant model of epistasis to explain the distribution of the different color variants observed (purple, brown, orange, yellow, and white). The presence of the white line may be controlled by a recessive allele with simple Mendelian traits on a locus distinct from those that control color variation.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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The shells of many marine mollusks show great diversity in colors and patterns of pigmentation. These variations, aside from their particular phenotypic effect, in some cases have been associated with differences in growth, survival, and other characteristics related to biological adaptations within species (Hoagland 1977; Mitton 1977; Walozek 1984; Wolff and Garrido 1991).
Variations in shell color have often been related to environmental effects (Cole 1975), but on other occasions they have been demonstrated to be genetically controlled. For example, black versus brown surfaces (Innes and Haley 1977; Mitton 1977) and banding patterns (Newkirk 1980) in Mytilus edulis, raylike marks on the surface of the clam Mercenaria mercenaria (Chanley 1961), basic color of the shell of Argopecten irradians (Adamkewicz and Castagna 1988), and the prismatic plates and nacre in the pearl oyster Pinctada fucata martensii (Wada and Komaru 1990) are controlled by allelic variations at one locus. Other characteristics, such as the pattern of distribution of pigmentation on the shell of A. irradians, appear to be controlled by the interaction of more than one pair of nonallelic genes (Adamkewicz and Castagna 1988).
The scallop of northern Chile and southern Peru, Argopecten purpuratus: Lamarck 1819, has a range of superficial shell colors, including white, yellow, orange, brown, and purple (Garrido 1990; Vildoso and Chirigno 1956; Wolff 1985; Wolff and Garrido 1991). The latter two colors are the most common ("normal") and are often represented by purple or brown blotches on a clear, usually white, background. A previous study showed that yellow-colored specimens experienced less growth and different responses to water temperature fluctuation when compared with specimens having "normal" coloration (Wolff and Garrido 1991). Also, Garrido (1990) found differences in growth parameters between orange specimens and "normally" colored specimens.
In hatchery production of large numbers of scallop juveniles ("seed"), further phenotypic characteristics related to shell coloring have been observed. One of interest to us is a dorsoventral white line appearing on the center of the left (upper) valve of many juvenile scallops. This marking, as well as the color polymorphism observed in the mass-produced hatchery populations, suggests that hereditary mechanisms control color patterns rather than environmental conditions.
A. purpuratus is a simultaneous hermaphrodite with external fertilization. It reproduces by liberating gametes to the environment, usually expelling sperm, followed by oocytes, by means of energetic pulsing of the valves (DiSalvo et al. 1984). This phenomenon permits separate collection of sperm and eggs, allowing for experimental self- and cross-fertilization such that even if the genotype of a specific locus in the progenitors is unknown, the phenotypes of the progeny may allow inferences concerning loci if suitable genetic markers are available (Adamkewicz and Castagna 1988). The present study analyzes the hereditary basis of general color polymorphisms in the shell of A. purpuratus on the basis of the results obtained by carrying out experimentally directed crosses.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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The pattern of shell color inheritance in A. purpuratus was studied by analyzing the phenotypic frequencies obtained from observing the characteristics of progeny produced by cross- and self-fertilization. Wild-caught adult specimens (broodstock) were obtained from Tongoy Bay (30°15'S) and Mejillones Bay (23°06'S) on the Chilean coast. Details concerning the phenotypes and origin of the broodstock employed are given in Table 1. Given the deleterious effects of encrusting organisms and the damage caused by the boring polychaete Polydora sp. on wild-caught broodstock, brown individuals could often not be distinguished from purple ones, both of which constitute the "normal" or most commonly seen morphs of the species. Broodstock was conditioned using procedures routinely employed in scallop hatcheries (DiSalvo et al. 1984), and spawning was artificially induced by removing them from the water for 30 min, followed by immersion in dense microalgal cultures as described by DiSalvo et al. (1984). In experiments with cross-fertilization, only oocytes from the fifth expulsion pulse onward were collected, where self-fertilization was 1% or less, following the method of Estévez (1992). Male and female gametes were collected separately from each individual, and fertilization was carried out using about seven spermatozoa per oocyte.
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Larval culture was carried out according to DiSalvo et al. (1984), with water changed every 2 days and feeding daily using about 30,000 cells/ml of Isochrysis tahitiensis. Larval culture was carried out in 30 L cylindrical fiberglass tanks (crosses 1–4 and 8–11) and in 500 L conical tanks (crosses 5–7 and 12). For crosses 1–4 and 8–11, "netlon" spat collectors were introduced after 18 days of culture at 21°C, and were then maintained for 60 days with partial water changes daily and ad libitum feeding with artificially cultured I. tahitiensis and Chaetoceros spp. After the initial culture period, scallop juveniles were removed from the spat collectors ("onion bags") and cultivated on the bottom of rectangular hatchery tanks receiving flow-through seawater until they reached size at which shell color and pattern were clearly distinguishable. For crosses 5–7 and 12, larvae of approximately 220–240 µm in length were separately collected from each cross in plastic bags in seawater and taken to the natural environment for setting (Garrido 1990). Later these juveniles were harvested and transferred to "pearl nets," where they were outcultured using locally employed scallop culture methods until they reached a size where shell color and pattern were fully distinguishable.
The offspring from each cross were classified according to the color of the left (upper) valve. The proportions of each morph in the progeny were compared with that expected assuming a simple dominant epistatic model with two interacting loci. The parental genotypes were inferred from the parental and progeny phenotypes. The fit of the phenotypic frequencies to the expected under the proposed model of inheritance were tested using the chi-squared test for goodness-of-fit. Yates's correction was used when the degree of freedom (df) was 1 (Zar 1974).
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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The different colors encountered in juvenile specimens of the northern scallop are shown in Figure 1, and include purple and brown ("normal" morphs), as well as orange, yellow, and white. "Normal" colors may show a range of tonalities, given the presence of white, brown, or other dark ornamentation.
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In the experiments conducted with normally colored broodstock from Tongoy Bay (crosses 1–5 with cross-fertilization and 8–11 with self-fertilization) we found purple, brown, yellow, and white juveniles, but none which was orange in color (Table 2). Orange specimens were only observed in crosses made with broodstock of this color (crosses 6, 7, and 12) (Table 2). Given that each family was maintained in a common environment, it was assumed that color variation was not attributable to environmental effects. These results are in agreement with other data available for marine bivalve species which postulate a hereditary basis for color variation of the shell surface (Adamkewicz and Castagna 1988; Chanley 1961; Innes and Haley 1977; Mitton 1977; Wada and Komaru 1990).
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In progeny arising from crosses of "normal" color broodstock, where no orange specimens were involved, the proportion of purple juveniles to all other colors was 3:1, except in crosses 1 and 5 (Table 2). Of these, in cross 1 the proportion was 1:1 (P > .1), while in cross 5 there occurred no simple Mendelian relation, with a relative excess of purple individuals (P < .01). The deviation of the phenotypic frequencies from the expected 3:1 proportions in cross 5 could be caused, at less partially, by the different experimental settling methodology. It is possible that larvae from the natural population recruit on the settling bags, producing an excess of normally colored seeds. Indeed, results are consistent with a model of one locus with one dominant allele which produces the purple color, and another allele, which is recessive, that permits expression of the other colors (brown, yellow, and white).
The proportion of brown juveniles in relation to yellow and white (where these appear) also shows significant adjustment to the 3:1 ratio, with the single exception of cross 5 (Table 2). Deviations in phenotypic frequencies in this cross can be caused by the same mechanism as purple color. This suggests that brown color is controlled by a different locus than purple color, with at least three alleles: one dominant, determinant of the brown color, and another two recessive, determinant of white and yellow color. Yellow and white individuals were never encountered together among the progeny of these crosses, which is in agreement with the concept of segregation on the same locus of alleles for yellow and white with respect to the allele that controls the expression of brown color. Purple individuals as well as brown ones showed a pigmentation pattern characterized by pigmented blotches on a clear (white) background, a characteristic not seen in yellow or white individuals. In general qualitative terms, the degree of coverage of these blotches varied among individuals within the same family.
The phenotypic proportions obtained suggested that the variation of color in A. purpuratus was controlled by a system of at least two interacting loci. The brown tone depended on the action of a dominant gene (M), while the colors yellow and white depended on the effects of recessive alleles M, my (yellow), and mw (white) at the same locus. The results from cross 6 (Table 2) suggest that the allele that determined the white color of the shell (mw) could be dominant over the yellow color (my) (P > .05), however, the number of crosses made and individuals examined was insufficient to arrive at a definitive conclusion on this point. The presence of the purple color may depend on the action of a dominant allele (P) on a second locus, epistatic over the loci governing the expression of the colors brown, yellow, and white (p). The presence of a recessive allele at this locus may permit the expression of the genes that cause the variation of color controlled by the hypostatic locus M. This model is in agreement with the phenotypic proportion 12:3:1 encountered in the experiments carried out using only parents of "normal" color (Table 2), and thus represented a simple dominant epistatic model of inheritance. The results of cross 1 were in agreement with this model if it is presumed that one of the parents was a heterozygote for the locus controlling purple color, while the other was a recessive homozygote for the allele of brown color, which permitted the expression of the other colors (P > .1).
Progeny from crosses involving orange-colored broodstock did not show patterns of color frequencies which fit the simple model of one or two loci interacting with a few segregating alleles. In cross 12 (self-fertilization), where no purple variants appeared, there was good adjustment to a 3 brown:1 orange ratio (Table 2; P > .1). This result, however, does not agree with the expected phenotypes based on the parental shell color. The results from cross 6, produced from two orange specimens, showed adjustment to the ratio of 3 purple:1 other, but they also did not agree with the expected phenotypes based on the parents' shell color. This cross pointed out the number of distinct color classes of the shells (four), suggesting the participation of more than two loci interacting in the control of this variation. A simple model of inheritance was likewise discounted on observing the results of cross 7 between orange and "normal" parents. These results clearly suggested a hereditary basis for the presence of the orange shell color, but emphasized the need for more extensive research to clarify its hereditary mechanism.
In all the crosses studied, except for cross 3, some juvenile scallops having a white line dorsoventrally crossing the center of the left (upper) valve were observed (Figure 1). The presence of this line on the shell remained stable during the 8 months of our observations, and only appeared or disappeared late in small numbers of specimens. In four of seven cross-fertilization experiments and three of four self-fertilizations, the proportion of individuals without the line to those with the line was 3:1 (P > .05). These results suggest that this character could be controlled by a locus with a pair of alleles with simple dominance for absence of the line. The results of cross 3 (Table 3) are consistent with this hypothesis of inheritance if one or both parents had been homozygous dominants for absence of the white line, resulting in progeny without the character. Crosses 5 and 6 were settled in the sea and their progeny could have been contaminated by wild larvae. This could explain why their results do not fit with expected frequencies under a simple one-locus Mendelian model of inheritance. However, the chance that 16 of 18 individuals randomly sampled from a population that is heterozygous is low. Indeed, the proposed hypothesis must be tested with a more extensive set of data.
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The existence of a possible association between the presence of the white line and the general coloration of the valve was examined in crosses 1–4 and 8–11. There was no significant association between shell color and the presence of the central line (P > .05) except in two crosses (.01 < P < .025).
Our results confirm the genetic basis for variation in shell color of A. purpuratus and suggest the existence of a simple dominant epistasis model that controls the general pattern of coloration in this species. A characteristic ornamentation of the shell, the central line, may be under the control of a third locus, independently segregated from genes which regulate overall shell color.
The low frequency of the yellow color morphs in natural populations of this species (Wolff and Garrido 1991) may be explained by the recessive condition of the alleles which regulate their expression and by dominant epistatic action exerted by the locus controlling the purple color. Thus the higher frequency of yellow individuals in cultured populations can be attributed in part to the high rates of self-fertilization typically present when this species is artificially reproduced in aquaculture (Estévez 1992). This, together with a lower mortality in cultures than in natural populations where the less frequent color morphs may be less viable under normal environmental conditions (Wolff and Garrido 1991), may increase the probability of expression in homozygosity of recessive and/or hypostatic alleles.
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Acknowledgments |
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The authors thank Dr. M. Wolff for help and suggestions during this study, and Dr. A. Sanjuan and two anonymous referees, whose critical readings and suggestions helped to improve this article. This work was financed through project no. 021 of the Office of Research of the Universidad Católica del Norte (DGIAT-UCN).
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Footnotes |
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Corresponding Editor: Masatoshi Nei
Received March 6, 2000
Accepted June 30, 2001
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References |
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