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BMC Evol Biol
2020 Aug 11;201:101. doi: 10.1186/s12862-020-01667-8.
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Distant hybrids of Heliocidaris crassispina (♀) and Strongylocentrotus intermedius (♂): identification and mtDNA heteroplasmy analysis.
Zhan Y
,
Sun J
,
Li Y
,
Cui D
,
Zhang W
,
Yang L
,
Chang Y
.
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BACKGROUND: Distant hybridization between the sea urchin Heliocidaris crassispina (♀) and the sea urchin Strongylocentrotus intermedius (♂) was successfully performed under laboratory conditions. A new variety of hybrid sea urchin (HS hybrid) was obtained. However, the early-development success rates for the HS hybrids were significantly lower than those of purebred H. crassispina or S. intermedius offspring. In addition, it was difficult to distinguish the HS-hybrid adults from the pure H. crassispina adults, which might lead to confusion in subsequent breeding attempts. In this study, we attempted to develop a method to quickly and effectively identify HS hybrids, and to preliminarily investigate the molecular mechanisms underlying the poor early-development success rates in the HS hybrids.
RESULTS: The hybrid sea urchins (HS hybrids) were identified both morphologically and molecularly. There were no significant differences in the test height to test diameter ratios between the HS hybrids and the parents. The number and arrangement of ambulacral pore pairs in the HS hybrids differed from those of the parental lines, which might serve as a useful morphological character for the identification of the HS hybrids. A primer pair that identified the HS hybrids was screened by comparing the mitochondrial genomes of the parental lines. Moreover, paternal leakage induced mitochondrial DNA heteroplasmy in the HS hybrids, which might explain the low rates of early development success in these hybrids.
CONCLUSIONS: The distant-hybrid sea urchins were accurately identified using comparative morphological and molecular genetic methods. The first evidence of mtDNA heteroplasmy after the distant hybridization of an echinoderm was also provided.
Fig. 1. Rate of success at each developmental stage in Heliocidaris crassispina purebred offspring, Strongylocentrotus intermedius purebred offspring, and H. crassispina (♀) × S. intermedius (♂) hybrids. HC_F: Purebred offspring of the H. crassispina Fujian population; SI_C: Purebred offspring of the S. intermedius cultured population; HS: H. crassispina (♀) × S. intermedius (♂) hybrids. “**” indicates an extremely significant difference (P < 0.01) between the two groups connected by the line
Fig. 2. Morphological comparisons among living individuals. HC_F: Heliocidaris crassispina Fujian population; SI_C: Strongylocentrotus intermedius cultured population; HS hybrid: H. crassispina (♀) × S. intermedius (♂) hybrids
Fig. 3. Ambulacral pore pair arrangements and numbers. a: Aboral side of test, Heliocidaris crassispina Fujian population; b: Aboral side of test, Strongylocentrotus intermedius cultured population; c: Aboral side of test, H. crassispina (♀) × S. intermedius (♂) hybrid. a: Ambulacral pore pairs, H. crassispina Fujian population; b: Ambulacral pore pairs, S. intermedius cultured population; c: Ambulacral pore pairs, H. crassispina (♀) × S. intermedius (♂) hybrids
Fig. 4. Amplification of mtDNA in Heliocidaris crassispina (♀) and Strongylocentrotus intermedius (♂) hybrids. a: Mitochondrial genome map for the H. crassispina Fujian population. b: Mitochondrial genome map for the S. intermedius cultured population. c: mtDNA fragment amplification diagram for the H. crassispina (♀) × S. intermedius (♂) hybrids. Primer pair V was selected for detection and identification; the product amplified by primer pair V is boxed in red. HC_F: H. crassispina Fujian population; SI_C: S. intermedius cultured population; HS hybrid: H. crassispina (♀) × S. intermedius (♂) hybrid. d. Electrophoresis gels, showing the results of PCR amplification using primer pairs that were used to amplify mtDNA fragments from the cultured population of S. intermedius. The fragments in the inner ring are more similar to the female parent (H. crassispina), while the fragments in the outer ring are more similar to the male parent (S. intermedius). The PCR products amplified by primer pair V, which was selected for identification, are boxed in red
Fig. 5. Genetic distance analysis. a: Mean distances among common sea urchins for 13 mitochondrial protein-coding genes; standard error is given in brackets. b: Genetic distance between the mitochondrial protein-coding genes of different pairs of populations. HC_F: Heliocidaris crassispina Fujian population; SI_C: Strongylocentrotus intermedius cultured population; HC_K: H. crassipina Korean population; SI_K: S. intermedius Korean population; SD: Strongylocentrotus droebachiensis; SP: strongylocentrotus purpuratus; HP: Hemicentrotus pulcherrimus; MN: Mesocentrotus nudus; GC: Glyptocidaris crenularis
Fig. 6. Identification of the Heliocidaris crassispina (♀) × Strongylocentrotus intermedius (♂) hybrids. a: 30 H. crassispina from the Fujian population. Electrophoresis gel, showing the PCR products amplified using the identification primer pairs. b: 30 H. crassispina (♀) × S. intermedius (♂) hybrids. Electrophoresis gel, showing the PCR products amplified using the identification primer pair
Fig. 7. Enzyme digestion of fragments from the parents of the Heliocidaris crassispina (♀) × Strongylocentrotus intermedius (♂) hybrids and from the pure offspring at each developmental stage. a: A 584 bp region was PCR amplified using total DNA as a template. The amplified fragment from the male parent (S. intermedius) contains an EcoR I-sensitive site. Thus, digestion of this PCR product produces two fragments (428 and 156 bp). However, the amplified fragment from the female parent (H. crassispina) is EcoR I-resistant. b: The fragments amplified from paternal mtDNA can be selectively digested and thus distinguished from the fragments amplified from maternal mtDNA (H. crassispina). Lane 1: PCR product resulting from maternal mtDNA amplification. This product could not be digested by the EcoR I restriction enzyme and was thus 584 bp long. Lane 2: PCR product resulting from paternal mtDNA amplification was successfully digested by the EcoR I restriction enzyme to produce 428 and 156 bp fragments. Lanes 3–5: the biparental mtDNA signal was detected at each stage. HC_F: H. crassispina Fujian population; SI_C: S. intermedius cultured population; HS hybrids: H. crassispina (♀) × S. intermedius (♂) hybrid
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