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Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species.

Chen S, Costa V, Beja-Pereira A - BMC Evol. Biol. (2011)

Bottom Line: Here we argue that neither ancestral polymorphism nor introgressive hybridization alone can fully account for haplotype sharing among species from Bos and Bison, and that both scenarios have contributed to such a pattern of haplotype sharing observed here.Additionally, codon-based tests revealed strong evidence for purifying selection in the Zp3 coding haplotype sequences and weak evidence for purifying selection in the Zp2 coding haplotype sequences.Contrary to a general genetic pattern that genes or genomic regions contributing to reproductive isolation between species often evolve rapidly and show little or no gene flow between species, these results demonstrate that, particularly, those sequenced exons of the Zp2 and the Zp3 did not show any contribution to reproductive isolation between the bovine species studied here.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.

ABSTRACT

Background: It has been established that mammalian egg zona pellucida (ZP) glycoproteins are responsible for species-restricted binding of sperm to unfertilized eggs, inducing the sperm acrosome reaction, and preventing polyspermy. In mammals, ZP apparently represents a barrier to heterospecific fertilization and thus probably contributes to reproductive isolation between species. The evolutionary relationships between some members of the tribe Bovini are complex and highly debatable, particularly, those involving Bos and Bison species for which interspecific hybridization is extensively documented. Because reproductive isolation is known to be a major precursor of species divergence, testing evolutionary patterns of ZP glycoproteins may shed some light into the speciation process of these species. To this end, we have examined intraspecific and interspecific genetic variation of two ZP genes (Zp2 and Zp3) for seven representative species (111 individuals) from the Bovini tribe, including five species from Bos and Bison, and two species each from genera Bubalus and Syncerus.

Results: A pattern of low levels of intraspecific polymorphism and interspecific divergence was detected for the two sequenced fragments each for Zp2 and Zp3. At intraspecific level, none of neutrality tests detected deviations from neutral equilibrium expectations for the two genes. Several haplotypes in both genes were shared by multiple species from Bos and Bison.

Conclusions: Here we argue that neither ancestral polymorphism nor introgressive hybridization alone can fully account for haplotype sharing among species from Bos and Bison, and that both scenarios have contributed to such a pattern of haplotype sharing observed here. Additionally, codon-based tests revealed strong evidence for purifying selection in the Zp3 coding haplotype sequences and weak evidence for purifying selection in the Zp2 coding haplotype sequences. Contrary to a general genetic pattern that genes or genomic regions contributing to reproductive isolation between species often evolve rapidly and show little or no gene flow between species, these results demonstrate that, particularly, those sequenced exons of the Zp2 and the Zp3 did not show any contribution to reproductive isolation between the bovine species studied here.

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The median-joining network (a) and geographic distribution (b) of the Zp3 coding haplotypes. Numbering of mutations follows the full coding sequence of the bovine Zp3 gene (from base 1 to 1266). The 6-bp insertion (or two-codon repeat) is located at the relative positions between 609 and 620 or between 603 and 604. Nonsynonymous mutations are shown in bold and italic. The size of each circle is proportional to its frequency in numbers of chromosomes. The haplotypes Zp3cdh14 and Zp3cdh15 from the outgroup species are not shown in the geographic map.
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Figure 3: The median-joining network (a) and geographic distribution (b) of the Zp3 coding haplotypes. Numbering of mutations follows the full coding sequence of the bovine Zp3 gene (from base 1 to 1266). The 6-bp insertion (or two-codon repeat) is located at the relative positions between 609 and 620 or between 603 and 604. Nonsynonymous mutations are shown in bold and italic. The size of each circle is proportional to its frequency in numbers of chromosomes. The haplotypes Zp3cdh14 and Zp3cdh15 from the outgroup species are not shown in the geographic map.

Mentions: There were eight coding haplotypes from the 222 bp coding sequence fragment of the Zp2 gene, of which the haplotypes Zp2cdh1 and Zp2cdh2 were predominant and shared by four and five bovine species, respectively (Figure 2a). Noticeably, only three haplotypes were identified in 194 chromosomes of five species from Bos and Bison. For the Zp3 gene, 15 coding haplotypes were defined by 19 coding SNPs (plus the two-codon repeat) in the 198 bp coding sequence fragment, of which one predominant haplotype Zp3cdh1 occurred 155 times, shared by B. taurus, B. indicus and B. frontalis (Figure 3a). Interestingly, there was no any single nonsynonymous mutation detected in, at least, 10 mutation steps from the Zp3cdh1 to the two outgroup species, i.e., the domestic sheep and goat (Figure 3a).


Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species.

Chen S, Costa V, Beja-Pereira A - BMC Evol. Biol. (2011)

The median-joining network (a) and geographic distribution (b) of the Zp3 coding haplotypes. Numbering of mutations follows the full coding sequence of the bovine Zp3 gene (from base 1 to 1266). The 6-bp insertion (or two-codon repeat) is located at the relative positions between 609 and 620 or between 603 and 604. Nonsynonymous mutations are shown in bold and italic. The size of each circle is proportional to its frequency in numbers of chromosomes. The haplotypes Zp3cdh14 and Zp3cdh15 from the outgroup species are not shown in the geographic map.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3037879&req=5

Figure 3: The median-joining network (a) and geographic distribution (b) of the Zp3 coding haplotypes. Numbering of mutations follows the full coding sequence of the bovine Zp3 gene (from base 1 to 1266). The 6-bp insertion (or two-codon repeat) is located at the relative positions between 609 and 620 or between 603 and 604. Nonsynonymous mutations are shown in bold and italic. The size of each circle is proportional to its frequency in numbers of chromosomes. The haplotypes Zp3cdh14 and Zp3cdh15 from the outgroup species are not shown in the geographic map.
Mentions: There were eight coding haplotypes from the 222 bp coding sequence fragment of the Zp2 gene, of which the haplotypes Zp2cdh1 and Zp2cdh2 were predominant and shared by four and five bovine species, respectively (Figure 2a). Noticeably, only three haplotypes were identified in 194 chromosomes of five species from Bos and Bison. For the Zp3 gene, 15 coding haplotypes were defined by 19 coding SNPs (plus the two-codon repeat) in the 198 bp coding sequence fragment, of which one predominant haplotype Zp3cdh1 occurred 155 times, shared by B. taurus, B. indicus and B. frontalis (Figure 3a). Interestingly, there was no any single nonsynonymous mutation detected in, at least, 10 mutation steps from the Zp3cdh1 to the two outgroup species, i.e., the domestic sheep and goat (Figure 3a).

Bottom Line: Here we argue that neither ancestral polymorphism nor introgressive hybridization alone can fully account for haplotype sharing among species from Bos and Bison, and that both scenarios have contributed to such a pattern of haplotype sharing observed here.Additionally, codon-based tests revealed strong evidence for purifying selection in the Zp3 coding haplotype sequences and weak evidence for purifying selection in the Zp2 coding haplotype sequences.Contrary to a general genetic pattern that genes or genomic regions contributing to reproductive isolation between species often evolve rapidly and show little or no gene flow between species, these results demonstrate that, particularly, those sequenced exons of the Zp2 and the Zp3 did not show any contribution to reproductive isolation between the bovine species studied here.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.

ABSTRACT

Background: It has been established that mammalian egg zona pellucida (ZP) glycoproteins are responsible for species-restricted binding of sperm to unfertilized eggs, inducing the sperm acrosome reaction, and preventing polyspermy. In mammals, ZP apparently represents a barrier to heterospecific fertilization and thus probably contributes to reproductive isolation between species. The evolutionary relationships between some members of the tribe Bovini are complex and highly debatable, particularly, those involving Bos and Bison species for which interspecific hybridization is extensively documented. Because reproductive isolation is known to be a major precursor of species divergence, testing evolutionary patterns of ZP glycoproteins may shed some light into the speciation process of these species. To this end, we have examined intraspecific and interspecific genetic variation of two ZP genes (Zp2 and Zp3) for seven representative species (111 individuals) from the Bovini tribe, including five species from Bos and Bison, and two species each from genera Bubalus and Syncerus.

Results: A pattern of low levels of intraspecific polymorphism and interspecific divergence was detected for the two sequenced fragments each for Zp2 and Zp3. At intraspecific level, none of neutrality tests detected deviations from neutral equilibrium expectations for the two genes. Several haplotypes in both genes were shared by multiple species from Bos and Bison.

Conclusions: Here we argue that neither ancestral polymorphism nor introgressive hybridization alone can fully account for haplotype sharing among species from Bos and Bison, and that both scenarios have contributed to such a pattern of haplotype sharing observed here. Additionally, codon-based tests revealed strong evidence for purifying selection in the Zp3 coding haplotype sequences and weak evidence for purifying selection in the Zp2 coding haplotype sequences. Contrary to a general genetic pattern that genes or genomic regions contributing to reproductive isolation between species often evolve rapidly and show little or no gene flow between species, these results demonstrate that, particularly, those sequenced exons of the Zp2 and the Zp3 did not show any contribution to reproductive isolation between the bovine species studied here.

Show MeSH
Related in: MedlinePlus