Heritable characteristics in the pearl oyster Pinctada martensii: comparisons of growth and shell morphology of Chinese and Indian populations, and reciprocal crosses.
Article Type: Report
Subject: Crassostrea (Demographic aspects)
Crassostrea (Physiological aspects)
Oysters (Demographic aspects)
Oysters (Physiological aspects)
Morphology (Animals) (Research)
Population genetics (Research)
Authors: Zhifeng, Gu
Yaohua, Shi
Yan, Wang
Aimin, Wang
Pub Date: 08/01/2011
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2011 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2011 Source Volume: 30 Source Issue: 2
Topic: Event Code: 310 Science & research
Product: Product Code: 0913050 Oysters NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: India; China Geographic Name: China; India Geographic Code: 9CHIN China; 9INDI India
Accession Number: 268309675
Full Text: ABSTRACT A complete diallel cross between two geographically distant pearl oyster (Pinctada martensii) populations, an Indian cultured population (I), and a Chinese cultured population (C) was carried out, and the resulting progenies (II, CC, IC, and CI) were cultured and studied for more than 700 days. Shell height and total weight were measured monthly, and shell thickness was measured in the middle and at the end of the experiment. The results reveal that II grew fastest whereas CC grew the slowest. The growth rate of reciprocal crosses CI and IC exhibited no statistically significant difference, with both appearing to be intermediate between the parental species, but superior to the mid parent values. The morphological traits of parents were inherited differently by the two reciprocal crosses. The traits of large size and relative thinness of shell from the Indian population were largely transmitted to CI, whereas relative small size and increased shell thickness of the Chinese population were mostly inherited by IC. The two parental stocks, the Indian population and the Chinese population, were unsuitable for commercial production because of a relatively thin shell and slow growth, respectively, but the reciprocal crosses combined desirable traits of the parents and exhibited considerable potential for commercial production and pearl culture.

KEY WORDS: pearl oyster, Pinctada martensii, diallel cross, genetic characteristics, morphology

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The marine pearl oyster Pinctada martensii is widely distributed throughout the equatorial zone, from the western Pacific Ocean (Korea and southern China), Australia, and the Indian Ocean to the Red Sea and the Persian Gulf, with Lessepsian migrants through the Suez Canal into the Mediterranean (Gervis & Sims 1992). It is commercially cultured in Japan, China, India, and Vietnam (Southgate & Lucas 2008) for the production of round pearls, popularly known as "Akoya pearls." These pearls are 5-10 mm in diameter and are most widely used in necklaces, especially the 14-16-inch choker and the 17-19-inch princess (Kripa et al. 2007). In China, P. martensii oysters were introduced from Japan to China in the 1960s and have been cultured for more than 40 y in 3 southern coastal provinces: Guangdong, Guangxi, and Hainan. The pearls produced by this species comprise more than 90% of the country's marine pearl production (Guo et al. 1999). In the past 2 decades, the production of Akoya pearls in China has increased dramatically. By the end of the 1980s and 1990s, its annual production was estimated to be more than 2 t and 20 t, respectively (Wang et al. 2007), and it reached 29.3 t in 2003 (Chen & Li 2007).

However since P. martensii oysters were first introduced from Japan more than 40 y ago, the only breeding method used by farmers has been selection, conducted in an informal manner with minimal assessment of efficacy. Because of the limited number of parents used for mating, genetic variation has been lost and inbreeding depression has arisen (Wang et al. 2003b, Deng et al. 2006, He et al. 2006), resulting in a decrease in oyster size and growth rate, which has directly affected the size of the nucleus and the value of the pearl. Therefore, P. martensii in China is in urgent need of genetic improvement to cultivate fast-growing and larger species.

Crossbreeding has been generally regarded as an effective way to realize genetic improvement by combining desirable characteristics found in one species with those of another (Hedgecock et al. 1995, Bryden et al. 2004, Zhang et al. 2004, Rahmana et al. 2005). Relevant studies has been reported in oysters (Newkirk et al. 1977, Newkirk 1980, Mallet & Haley 1983b, Mallet & Haley 1984, Newkirk 1986, Hawes et al. 1990, Hedgecock et al. 1995, Hedgecock et al. 1996, Bayne et al. 1999, Soletchnik et al. 2002, Pace et al. 2006, Hedgecock & Davis 2007), abalone (Wang & Fan 1999, Ke et al. 2000, Sun et al. 2001, Liu et al. 2003, Zhang et al. 2006), scallop (Cruz & Ibarra 1997, Chang et al. 2002, Li et al. 2002, Qin et al. 2007, Zhang et al. 2007), mussel (Koehn 1991), and hard clam (Manzi et al. 1991). Concerning the crossing of P. martensii, studies have been undertaken in Japan (Wada 1984, Wada & Komaru 1994), and have reported hybrid crosses superior to inbred crosses in survival and growth. However, in China (Wang et al. 2003a, Wang et al. 2004), crosses of geographically different populations from Guangdong, Guangxi, and Hainan were carried out, but no significant improvement in growth in was obtained.

In this study, a cross between two geographically distant populations an Indian population and a Chinese population--of P. martensii was conducted to determine whether there was a significant improvement in growth of reciprocal crosses from pure populations. In pearl production, shell height (SH) and shell thickness (ST) are the chief criteria in deciding whether oysters are appropriate for implantation, and the size of the nuclei that may be seeded. In China, oysters are considered mature enough for implantation when SH is 60 mm and they can be inserted with a nuclei of 6.5 mm. If the nuclei are larger, oysters should be larger, too (Gu et al. 2009). In addition to SH, ST is another criterion, because oysters with thin shells are unfit for implantation of large nuclei (Kripa et al. 2007). In this experiment, Indian and Chinese populations differ in morphology and growth rate, and are complementary in SH and ST. The Indian cultured population is large and fast growing; however, its shells are rather thin and fragile, and easy to crack during implantation, thus it is impossible to produce pearls larger than 5 mm (Kripa et al. 2007). In comparison, as observed by local farmers, the local Chinese population has thick, tough shells, but it is small and has a low growth rate, and hence is unfit for the implantation of large nuclei. The objective of this study was to explore the possibility of producing desirable traits such as faster growth and greater ST in the reciprocal crosses compared with intrapopulation crosses under identical culture systems.

MATERIALS AND METHODS

Study Site

The study was undertaken in Li'an Lagoon (18[degrees]24'1-18[degrees]27, N, 110[degrees]02'-110[degrees]04' E), Hainan Island, South China. This lagoon, stretching 4 km north to south and 2.8 km east to west, is linked with the ocean by a narrow branch 60 m wide in the southeast. The mean water temperature is around 26[degrees]C, ranging from 19-30[degrees]C (Gu et al. 2009); salinity is 31-34%0, with a water depth of 8.5 m and an average flow rate of 3 cm/sec at the farming location.

Breeding Design

In this experiment, the two parental stocks the Indian and Chinese populations produced 4 crosses: 2 intrapopulation crosses (II and CC; I, Indian; C, Chinese) and 2 reciprocal crosses (IC and CI). For consistency, when referring to the between-population crosses, the maternal species is named first.

The parental stocks of the Indian and Chinese populations were collected from a commercial farm in Li'an Lagoon, Hainan Island, and reared under identical conditions. The Indian group is the [F.sub.2] offspring of 200 oysters introduced from the Bay of Bengal along the southeast coast of India in 2002 to Hainan and reared in Li'an Lagoon for experiment. The Chinese Sanya group is cultured locally, whose ancestors are the wild pearl oysters distributed in the coastal waters of Sanya Bay, and have been reared commercially in Li'an Lagoon for more than 5 generations for pearl production.

On March 15, 2003, 80 2.5-y-old oysters from each population were collected and transported to the laboratory at Li'an, where they were cleaned and immersed in 5 ppm potassium permanganate for 5 min for disinfection (Wang et al. 2003a). Then, they were measured and further divided into males and females by pricking the gonad with a needle and observing the reproductive cells under a microscope. Last, 30 female and male oysters were chosen from each population as parents for breeding. The parameters of the parents are shown in Table 1.

The mating design is shown in Figure I. Males and females of one population were separately placed in two aerated tanks, each containing 200 L filtered seawater. All oysters were injected with 0.1 mL of 0.02 mM serotonin (5-droxytryptamine) (Sigma) into the adductor muscle to induce spawning (Zhang et al. 2007). Males were injected first, followed by females, because eggs have a shorter lifespan than sperm, and if eggs are exposed to the air for a long time, their quality may degrade. Around half an hour after injection, oysters began to spawn, and more than 80% of males and females participated in the production of offspring. After spawning, the sperm or the eggs in each tank were stirred and split into two halves. Then eggs were fertilized as shown in Figure 1, and 4 crosses were produced: II, CC, IC, and CI.

Larvae Rearing and Culture of Spat and Adults

The fertilized eggs were collected on a 38-[micro]m mesh sieve and reared in 1,000-L aerated fiberglass tanks for hatching. Four to 5 h after fertilization, when the fertilized eggs developed into trochophore larvae, aeration was stopped and the larvae were collected from the upper layer of the tanks and transferred to 30,000-L cement pits, where the density was maintained at 4 larvae/mL. When the eye spots appeared, polyethylene rope-type collectors were deployed into the larval tanks (Gervis & Sims 1992). After that, the rearing of spat was carried out using standard practices (Gu et al. 2009). When spat reached a 2.5-cm SH, they were transferred into circle nets with 2.0-cm mesh and were reared at a density of 200-300 spat per net. Thereafter, net changing, shell cleaning, and density adjustment were conducted regularly in accordance with normal commercial practice (Wada & Komaru 1991).

Because all oysters were farmed in natural waters, their growth might be easily affected by environmental factors--in particular, temporal differences in food abundance. To minimize such environmental effects, all oysters of the four crosses were arranged in a line in the same area normal to the direction of tidal currents. Specifically, the tidal currents in Li'an Lagoon flow from south to north, and the oyster nets of the 4 crosses were deployed along a 180-m east-west long-line, so that the oysters could obtain equal amounts of food brought by tidal currents.

Measurement and Statistical Analysis

The measurement of SH ([+ or -] 0.01 mm) was conducted from May 2003 to March 2005, whereas the measurement of total weight (TW; [+ or -] 0.01 g) began 1 mo later, because in May 2003, oysters were not heavy enough to allow for a weight measurement. A total of 100 oysters from each cross were randomly collected, cleaned, and then measured (Hwang et al. 2007). In addition to SH and TW, in January 2004 and March 2005, ST was also measured, and relative thickness was calculated by ST divided by SH.

[FIGURE 1 OMITTED]

Oysters are suitable for nucleus implantation when SH reaches 60 mm (Gu et al. 2009). Therefore, the numbers of oysters in the 4 groups with an SH more than 60 mm were calculated at different times.

One-way analysis of variance with a posteriori Tukey HSD tests were used to test the null hypothesis that the means of SH, ST, TW, or ST/SH in the 4 groups are equal at [alpha] = 0.01 (PASW Statistics, 2009).

RESULTS

Growth

The growth trends for SH and TW of four groups are shown in Figure 2B. The reciprocal crosses CI and IC were intermediate to their parental species, and comparatively much closer to their fast-growing parental Indian population. Both SH and TW of the reciprocal crosses were significantly larger than those of the slow-growing CC, but significantly smaller than the fast-growing II cross (P < 0.01) under identical rearing conditions (Tables 2 and 3). The two reciprocal crosses did not show a statistically significant difference in SH or TW (P > 0.05; Tables 2 and 3), except that on days 53 and 87, IC had a significantly larger SH than CI (P > 0.05).

Morphological Features

Four groups differed in morphology as well. Mean values of ST and ST/SH on days 300 and 727 (the end of the experiment) are summarized in Tables 2 and 3. On day 300, II had the largest ST but the smallest ST/SH, whereas CC had the smallest ST, but significantly larger ST/SH (Table 2). Therefore, in morphology, II was large but relatively thin, whereas CC was small but relatively thick. Reciprocal crosses IC and CI showed different traits, and on day 727, IC had a significantly higher ST/SH than CI (Table 3). The final results show that the ST/SH of the 4 crosses differed significantly (P < 0.01) from each other, but the values of the two reciprocal crosses were comparatively much closer to the thick parental Chinese population.

Proportion and Age of Pearl Oysters Fit for Implantation

Figure 3 shows the proportion and age of oysters (SH [greater than or equal to] 60 ram) large enough for implantation of the 4 groups. Oysters fit for implantation were observed to appear about 290 clays after fertilization. At the end of the experiment, II, CI, and IC had approximately 100% of oysters ready for implantation, but CC had only 45%. Of the 4 groups, the II group generally had the largest proportion of oysters suitable for implantation, followed by CI, IC, and CC. For example, on day 543, the percentages of II, CI, IC and CC were 80.6%, 62.5%, 40.5%, and 6% respectively.

[FIGURE 2 OMITTED]

DISCUSSION

Cross experiments of bivalves are well documented, but the conclusions are not always consistent. The hybridization of abalone revealed that the spawn rate, hatch rate, and larval survival rate of hybrid progeny were lower compared with a purebred cross (Wang & Fan 1999, Ke et al. 2000, Sun et al. 2001, He et al. 2007), but hybrids usually had a higher growth rate (Wang & Fan 1999, Ke et al. 2000, He et al. 2007). A similar conclusion was reached in the Pacific oyster (Lannan 1980, Beattie et al. 1987, Pace et al. 2006) and the American oyster (Mallet & Haley 1983a, Mallet & Haley 1983b). On the other hand, Mallet and Haley (1984) found that not all reciprocal crosses yielded superior growth performance, which was confirmed by Hedgecock et al. (1995) in the study of the Pacific oyster. Meanwhile, most cross experiments carried out in scallops in China reported a significant increase in both larval survival and growth of reciprocal crosses (Chang et al. 2002, Li et al. 2002, Zheng et al. 2004, Chang et al. 2006, Zhang et al. 2007).

In comparison, few studies have been conducted on the pearl oyster P. martensii except those by Wada and Komaru (1994) and Wang et al. (2003b, 2004). Wada and Komaru (1994) crossed pearl oysters of different shell coloration and found hybrid crosses superior to inbred crosses in survival and growth rates. Wang et al. (2003b, 2004) carried out crosses of three geographically different populations and found no significant improvement in growth. A possible reason for the lack of differences between these crosses might be a lack of genetic traits, because the three populations were collected from Guangdong, Guangxi, and Hainan, which are all located in the south of China. In the experiment by Wang et al. (2003b, 2004), after 18 months of rearing, the three intrapopulation crosses were almost the same in SH (47-48 cm), ST (19-20 cm), and TW (13-14 g). Not surprisingly, the 3 between-population crosses resembled each other in the 3 growth parameters. However, in the current study, the two parental stocks differed in geography, morphology, and genetic traits. The Indian population had a significantly larger SH, ST, and TW, and a significantly smaller relative ST/SH than the Chinese population (Table 1).

Hou et al. (2008) found high differentiation between the 2 parental populations (mean FST, 0.486), and a moderate level of genetic diversity. They also reported that the traits of the Indian and Chinese populations were highly complementary, and expected to show heterosis in between-population crosses. The results of the current study reveal that reciprocal crosses had superior performance over the mid-parent values and exhibited many desirable traits. Similar results were observed in scallop (Cruz & Ibarra 1997) and Pacific oyster (Soletchnik et al. 2002).

The two reciprocal crosses in the current study were variable and exhibited different features in growth and morphology. IC exhibited significantly faster SH than CI in the first 3 months, almost the same in the fourth month, was surpassed by CI in the fifth month, and maintained the same trend until the end of the experiment (Fig. 2A). Probably this variation was caused by maternal effects, which for most part are produced by both genotype and nongenetic factors of female breeders (Pirchner 1983). In the current study, the maternal effects probably lasted for 3 mo, because the SH results of the first 3 months suggested that the eggs from the Indian population resulted in larger oysters than the eggs from the Chinese population. However, reports on maternal effects from other sources diverge considerably. Most studies found that maternal effects are expected to have the greatest impact on traits during the early stages of development, especially at the larvae stage (Newkirk et al. 1977, Mallet & Haley 1984, Cruz & Ibarra 1997, Zhang et al. 2007). Bivalves are subject to a maternal effect during the first stages of their life (Pirchner 1983), because egg reserves are the principle determinant for early growth and survival (Cragg & Crisp 1991). Maternal effects usually fade away at older ages, and are sometimes balanced by compensatory growth in one of the reciprocal crosses (Cruz & Ibarra 1997). On the other hand, some studies also proved that the maternal effects extended to the juvenile stage or adulthood, as is the case in the current study, in which maternal effects lasted for about 2 mo. Soletchnik et al. (2002) reported that hybrids of cupped oysters had clear maternal effects for growth and reproductive characteristics by the end of the 17-mo experiment. In hybrids of Chinook salmon (Bryden et al. 2004), maternal effects were significant in the first and second year and then declined, but lasted to the third and fourth year. Bentsen et al. (1998) observed small but significant maternal effects at harvest of a diallel cross of tilapia strains. Therefore, persistence of maternal effects into the juvenile stage and adulthood is worthy of further investigation.

[FIGURE 3 OMITTED]

The purpose of crossbreeding is to achieve genetic improvement by retaining the favorable traits and minimizing the weakness of parental species. To be exact, in this study, the two parental populations varied in morphology and growth performance. The Indian population is large and fast growing with a relatively thin shell, whereas the Chinese population has a relatively thick shell but is small and slow growing. Both species are deficient in terms of appropriateness for nucleus implantation. The thin, fragile shell of the Indian cultured population complicates implantation and discourages attempts to produce pearls larger than 5 mm (Kripa et al. 2007), whereas the long culture period and small size of the Chinese population increases the costs of commercial production. Interestingly, through crossbreeding, the desirable characteristics--such as large size and fast growth of the Indian population, and large relative thickness of the Chinese population were inherited by the reciprocal crosses, and undesirable traits were reduced. Specifically, CI carried more features of the Indian group and gained a fast growth rate, and its ST/SH was also improved. On the contrary, IC was more similar to CC in ST, but superior to it in growth rate. Hence, both reciprocal crosses have considerable potential for commercial production and pearl culture.

ACKNOWLEDGMENTS

This study was supported by the National Basic Research Program of China (973 Program) (2010CB126405 and 2009CB126005); the Natural Science Foundation of Hainan (2010CB126405 and 2009CB126005); the Key Laboratory of Tropic Biological Resources; MOE, and Hainan Key Laboratory of Tropical Hydrobiological Technology.

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GU ZHIFENG, SHI YAOHUA, WANG YAN AND WANG AIMIN *

The Ocean College, Hainan University, Key Laboratory of Tropical Biological Resources, MOE, Hainan Key Laboratory of Tropical Hydrobiological Technology, Haikou 570228, P. R. China

* Corresponding author. E-mail: aimwang@163.com

DOI: 10.2983/035.030.0207
TABLE 1.
Numbers of parents and respective shell height, shell thickness,
total weight, and relative thickness.

                                   Shell
Population          n           Height (mm)

Indian population   60    92.72 [+ or -] 5.75 (A)
China population    60    68.75 [+ or -] 5.13 (B)

                              Shell
Population               Thickness (mm)

Indian population    29.91 [+ or -] 1.76 (A)
China population     26.77 [+ or -] 1.92 (B)

                              Total
Population                 Weight (g)

Indian population    82.89 [+ or -] 2.45 (A)
China population     46.24 [+ or -] 2.52 (B)

                            Relative
Population              Thickness (ST/SH)

Indian population    0.32 [+ or -] 0.02 (B)
China population     0.39 [+ or -] 0.03 (A)

All values represent mean [+ or -] SD. Mean values with the same
superscript are not significantly different (Tukey's test, P < 0.01).

TABLE 2.
Mean values of shell height, shell thickness, total weight, and
relative thickness of the 4 groups on day 300.

                                     300 days

                          Shell                       Shell
Group    n             Height (mm)               Thickness (mm)

II       225    45.25 [+ or -] 6.91 (A)     13.60 [+ or -] 2.13 (A)
IC       238    39.21 [+ or -] 6.87 (C)     12.79 [+ or -] 2.49 (B)
CI       215    41.60 [+ or -] 5.78 (B)     13.19 [+ or -] 2.03 (AB)
CC       264    32.46 [+ or -] 5.41 (D)     10.68 [+ or -] 1.89 (C)

                              300 days

                   Total                     Relative
Group           Weight (g)               Thickness (ST/SH)

II       10.24 [+ or -] 4.15 (A)     0.30 [+ or -] 0.03 (C)
IC        8.11 [+ or -] 3.85 (B)     0.33 [+ or -] 0.03 (AB)
CI        8.66 [+ or -] 3.35 (B)     0.32 [+ or -] 0.03 (B)
CC        4.96 [+ or -] 2.22 (C)     0.33 [+ or -] 0.03 (A)

All values represent mean [+ or -] SD. Mean values with the same
superscript are not significantly different (Tukey's test,
[alpha] = 0.01).

TABLE 3.
Mean values of shell height, shell thickness, total weight, and
relative thickness of the 4 groups on day 727.

                                    727 days

                         Shell                       Shell
Group    n            Height (mm)               Thickness (mm)

II       110   78.51 [+ or -] 8.67 (A)     25.99 [+ or -] 2.84 (A)
IC       128   70.84 [+ or -] 6.54 (B)     26.51 [+ or -] 3.09 (A)
CI       126   72.22 [+ or -] 8.12 (B)      25.9 [+ or -] 2.96 (A)
CC       131   58.88 [+ or -] 8.08 (C)      22.7 [+ or -] 2.93 (B)

                              727 days

                   Total                     Relative
Group           Weight (g)               Thickness (ST/SH)

II       55.93 [+ or -] 14.52 (A)    0.33 [+ or -] 0.03 (D)
IC       44.34 [+ or -] 10.34 (B)    0.37 [+ or -] 0.03 (B)
CI       48.79 [+ or -] 13.26 (B)    0.36 [+ or -] 0.03 (C)
CC       33.67 [+ or -] 11.14 (C)    0.39 [+ or -] 0.02 (A)

All values represent mean [+ or -] SD. Mean values with the same
superscript are not significantly different (Tukey's test, P < 0.01).
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