Abstract
Samples were collected from the subtidal region of Jumunjin on the eastern coast of Korea in July 2020. A total of 338 mussels of shell height (SH) 20.8–149.8 mm were used for sex ratio analysis. The sex ratio (F:M) in the same population of mussel Mytilus coruscus was approximately 1:0.7. The sex ratio according to the class of SH was different. The sex reversal pattern of M. coruscus appears to go from male → female → male → female, and as such is determined to be sequential hermaphrodites.
Keywords: Mytilus coruscus, Sequential hermaphroditism, Sex reversal
INTRODUCTION
In general, the determination of animal sex is based on their morphological sex. Sex of bivalves can be categorized as either gonochoristic or hermaphroditic, whereas hermaphrodites can be described as either simultaneous or sequential (Coe, 1943; Heller, 1993; Yusa, 2007). Sequential hermaphrodites undergo sex changes during their life cycle, and their morphological sex is expressed differently according to the life cycle stage. The identification of sequential hermaphroditism requires direct evidence of sex change (Coe, 1943; Lee et al., 2013, 2014). However, since obtaining direct evidence requires considerable time and effort, an indirect method is used to analyze the change in sex ratio according to age or size within the same population (Galtsoff, 1937; Guo et al., 1998; Eversole, 2001; Park et al., 2012). The purpose of this study was to analyze the sex ratio of the mussel Mytilus coruscus, which is known to be gonochoristic (Wi et al., 2003), to thus describe its sex changes and sex.
MATERIALS AND METHODS
Mussels were collected from the subtidal region of Jumunjin on the eastern coast of Korea in July 2020 (Fig. 1). A total of 338 mussels of shell height (SH) 20.8–149.8 mm were used for sex ratio analysis. Sex was confirmed by observing anatomical and microscopic tissue specimens (Fig. 2). The sex ratio was recorded by dividing into classes of SH 10.0 mm each. The sex ratio (F:M) was expressed as the ratio of males (M) to females (F) and the female proportion (%) of the total, and statistical analysis was performed using the Chi-square (χ2) test.
Fig. 1. Sampling area of Mytilus coruscus.
Fig. 2. Morphocharacteristics (A), anatomy and histology of gonad in Mytilus coruscus.
(B) female, (C) male. Oc, oocyte; SH, shell height; SL, shell length; Sp, sperm.
RESULTS AND DISCUSSION
The overall sex ratio of mussels was approximately 1:0.7. However, the sex ratio according to the class of SH was different, where the male proportion was high in classes of SH 20.1–50.0 mm, but the female proportion was high in the SH 50.1–70.0 mm classes. The ratio of males was higher again in the SH 70.1–80.0 mm class, whereas the ratio of females was higher in the above SH 80.1 mm classes (Table 1). These results indicate that mussels are sequential hermaphrodites that periodically change sex (♂ → ♀ → ♂ → ♀).
Table 1. Sex ratio with shell height of mussel Mytilus coruscus.
| Shell height (mm) | Number | Sex ratio (F:M) | Female (%) | Male (%) | Chi-square | p-value | Dominant sex | ||
|---|---|---|---|---|---|---|---|---|---|
| Total | Female | Male | |||||||
| 20.1–30.0 | 35 | 14 | 21 | 1:1.50 | 40.00 | 60.00 | 1.40 | 0.310 | ♂ |
| 30.1–40.0 | 35 | 16 | 19 | 1:1.19 | 45.71 | 54.29 | 0.26 | 0.737 | |
| 40.1–50.0 | 41 | 19 | 22 | 1:1.16 | 46.34 | 53.66 | 0.22 | 0.759 | |
| 50.1–60.0 | 57 | 30 | 27 | 1:0.90 | 52.63 | 47.37 | 0.16 | 0.795 | ♀ |
| 60.1–70.0 | 35 | 23 | 12 | 1:0.52 | 65.71 | 34.29 | 3.46 | 0.084 | |
| 70.1–80.0 | 16 | 6 | 10 | 1:1.67 | 37.50 | 62.50 | 1.00 | 0.461 | ♂ |
| 80.1–90.0 | 33 | 21 | 12 | 1:0.57 | 63.64 | 36.36 | 2.46 | 0.158 | ♀ |
| 90.1–100.0 | 36 | 24 | 12 | 1:0.50 | 66.67 | 33.33 | 4.00 | 0.061 | |
| 100.1–110.0 | 30 | 18 | 12 | 1:0.67 | 60.00 | 40.00 | 1.20 | 0.365 | |
| 110.1–120.0 | 32 | 28 | 4 | 1:0.14 | 87.50 | 12.50 | 18.00 | <0.001 | |
| 120.1–130.0 | 13 | 12 | 1 | 1:0.08 | 92.31 | 7.69 | 9.31 | 0.003 | |
| 130.1≤ | 14 | 12 | 2 | 1:0.17 | 85.71 | 14.29 | 7.14 | 0.012 | |
| Total | 377 | 223 | 154 | 1:0.69 | 59.15 | 40.85 | 12.63 | <0.001 | |
Sex change normally occurs during the gonadal inactive stage in bivalves include Crassostrea virginica, C. gigas, Ruditapes philippinarum and Tegillarca granosa (Thompson et al., 1996; Park et al., 2012; Lee et al., 2013, 2014). However, sex change in Patinopecten yessoensis occurs during the gonadal active stages (Osanai, 1975). Genetic and environmental factors such as temperature affect the sex determination and change of sex ratio in bivalves (Yusa, 2007). It was confirmed in this study that the sex ratio and change according to shell size of M. coruscus. Therefore, more detailed research is needed on the season and factors involved in the sex changes of M. coruscus.
Acknowledgements
Not applicable.
ORCID
Hyeon Jin Kim https://orcid.org/0000-0001-9208-4616
So Ryung Shin https://orcid.org/0000-0002-2888-1378
Han Young Oh https://orcid.org/0000-0001-8522-3913
Jae won Kim https://orcid.org/0000-0002-9035-6005
Jung Sick Lee https://orcid.org/0000-0001-6292-328X
Conflict of interests
The authors declare no potential conflict of interest.
Authors’ contributions
Conceptualization: Kim JW, Lee JS.
Data curation: Kim HJ, Shin SR.
Formal analysis: Kim HJ, Oh HY.
Methodology: Kim JW, Lee JS.
Software: Kim HJ, Shin SR.
Validation: Lee JS, Kim JW.
Investigation: Kim HJ, Shin SR, Oh HY, Kim JW.
Writing-original draft: Kim HJ, Lee JS.
Writing-review & editing: Kim HJ, Shin SR, Lee JS.
Ethics approval
This article does not require IRB/IACUC approval because there are no human and animal participants.
References
- Coe WR. Sexual differentiation in mollusks. I. Pelecypods. Q Rev Biol. 1943;18:154–164. doi: 10.1086/394673. [DOI] [Google Scholar]
- Eversole AG. Reproduction in Mercenaria mercenaria. Biology of the Hard Clam. In: Kraeuter JN, Castagna M, editors. Elsevier; New York, NY: 2001. pp. 221–260. (eds) [DOI] [Google Scholar]
- Galtsoff PS. Observations and experiments on sex change in the adult American oyster, Ostrea virginica. Collect Net. 1937;12:187. [Google Scholar]
- Guo X, Hedgecock D, Hershberger WK, Cooper K, Allen SK., Jr Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution. 1998;52:394–402. doi: 10.2307/2411076. [DOI] [PubMed] [Google Scholar]
- Heller J. Hermaphroditism in molluscs. Biol J Linn Soc. 1993;48:19–42. doi: 10.1111/j.1095-8312.1993.tb00874.x. [DOI] [Google Scholar]
- Lee JS, Park JJ, Shin YK, Kim H, Jeon MA. Sex change and sequential hermaphroditism in Tegillarca granosa (Bivalvia: Arcidae) Invertebr Reprod Dev. 2014;58:314–318. doi: 10.1080/07924259.2014.949014. [DOI] [Google Scholar]
- Lee JS, Park JS, Shin YK, Lee YG, Park JJ. Sequential hermaphroditism in Manila clam Ruditapes philippinarum (Bivalvia: Veneridae) Invertebr Reprod Dev. 2013;57:185–188. doi: 10.1080/07924259.2012.717109. [DOI] [Google Scholar]
- Osanai K. Seasonal gonad development and sex alteration in the scallop, Patinopecten yessoensis. Bull Mar Biol Stn Asamushi Tokyo Univ. 1975;15:81–88. [Google Scholar]
- Park JJ, Kim H, Kang SW, An CM, Lee SH, Gye MC, Lee JS. Sex ratio and sex reversal in two-year-old class of oyster, Crassostrea gigas (Bivalvia: Ostreidae) Dev Reprod. 2012;16:385–388. doi: 10.12717/DR.2012.16.4.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson RJ, Newell RIE, Kennedy VS, Mann R. Reproductive process and early development. The Eastern Oyster: Crassostrea virginica. In: Kennedy VS, Newell RIE, Eble AF, editors. Maryland Sea Grant, College Park; MD: 1996. pp. 335–370. (eds) [Google Scholar]
- Wi CH, Chang YJ, Lee SJ, Hur YB, Lee JS. Sexual maturation and gametogenic cycle of the hard shelled mussel, Mytilus coruscus (Bivalvia: Mytilidae) Aquaculture. 2003;16:245–251. [Google Scholar]
- Yusa Y. Causes of variation in sex ratio and modes of sex determination in the Mollusca: An overview. Am Malacol Bull. 2007;23:89–98. doi: 10.4003/0740-2783-23.1.89. [DOI] [Google Scholar]