Limits...
Copy number variation in the speciation of pigs: a possible prominent role for olfactory receptors.

Paudel Y, Madsen O, Megens HJ, Frantz LA, Bosse M, Crooijmans RP, Groenen MA - BMC Genomics (2015)

Bottom Line: Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation.Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species.These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs).

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen University, 6700 AH, Wageningen, The Netherlands. paudelyogesh@gmail.com.

ABSTRACT

Background: Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation. Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species. Previous studies provided detailed knowledge on the potential evolutionary role of SVs, especially copy number variations (CNVs), between well diverged species of e.g. primates. However, our understanding of their significance during ongoing speciation processes is limited due to the lack of CNV data from closely related species. The genus Sus (pig and its close relatives) which started to diverge ~4 Mya presents an excellent model for studying the role of CNVs during ongoing speciation.

Results: In this study, we identified 1408 CNV regions (CNVRs) across the genus Sus. These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs). The majority of these copy number variable genes are olfactory receptors (ORs) known to play a prominent role in food foraging and mate recognition in Sus. Phylogenetic analyses, including novel Bayesian analysis, based on CNVRs that overlap ORs retain the well-accepted topology of the genus Sus whereas CNVRs overlapping genes other than ORs show evidence for random drift and/or admixture.

Conclusion: We hypothesize that inter-specific variation in copy number of ORs provided the means for rapid adaptation to different environments during the diversification of the genus Sus in the Pliocene. Furthermore, these regions might have acted as barriers preventing massive gene flow between these species during the multiple hybridization events that took place later in the Pleistocene suggesting a possible prominent role of ORs in the ongoing Sus speciation.

No MeSH data available.


Simple schematic diagram of tested constrained models. A: Constrained model 1 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus celebensis. B: Constrained model 2 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus verrucosus. C: Constrained model 3 where other species consists of Sus scrofa (Europe and China) and Sus cebifrons, Sus celebensis and Sus verrucosus. D: Constrained model 4 where other species consists of Sus scrofa (Sumatra and Europe) and Sus barbatus, Sus celebensis and Sus verrucosus.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4413995&req=5

Fig5: Simple schematic diagram of tested constrained models. A: Constrained model 1 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus celebensis. B: Constrained model 2 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus verrucosus. C: Constrained model 3 where other species consists of Sus scrofa (Europe and China) and Sus cebifrons, Sus celebensis and Sus verrucosus. D: Constrained model 4 where other species consists of Sus scrofa (Sumatra and Europe) and Sus barbatus, Sus celebensis and Sus verrucosus.

Mentions: To further evaluate the discrepancies between the different partitions we performed a more parametric phylogenetic approach, Bayesian phylogenetic analysis, using the MKV model [42] as implemented in MrBayes v2.2 [43], and an extending encoding of the CNs. We first ran the MKV model without any topology constrains and found that the monophyly of the Sus-ISEA and Sus scrofa clades, as identified by the SNP data and in previous analyses [31], was highly supported (posterior probability PP > 0.9) for both CNVR-OR and CNVR-ALL, but not for CNVR-nonOR which supported a Sus cebifons and Sus scrofa (China) relationship. To address the strength of support for these discrepancies we tested different constrained models that fit the history of inter-specific admixture [31]. We first computed the support (marginal likelihood; see methods) for a model in which the monophyly of Sus-ISEA and Sus scrofa clades were constrained, a scenario consistent with the SNP tree. Thereafter 4 different models were tested that are described in Figure 5 A-D. In Model-1, we constrained Sus verrucosus and Sus scrofa Sumatra to be monophyletic (Figure 5A), representing known admixture among these species [31]. In Model-2, we constrained Sus celebensis and Sus scrofa Sumatra to be monophyletic (Figure 5B) representing possible human translocations of Sus celebensis to Sumatra and neighboring islands. In Model-3, Sus barbatus and Sus scrofa Sumatra were constrained to be monophyletic (Figure 5C), representing known admixture between these two species/populations. In Model-4, Sus cebifrons and Sus scrofa China were constrained to be monophyletic (Figure 5D), representing possible migration from MSEA to the Philippines [31]. The marginal likelihood analysis strongly supports the monophyly of the two major clade of Sus-ISEA and Sus scrofa for CNVR-OR and CNVR-ALL but not for CNVR-nonOR where this monophyly provides a much poorer fit. For CNVR-nonOR the difference in marginal likelihood (delta-lnL) to the model was 7.46 (Table 2), which strongly supports the non-monophyly of the two major clades.Figure 5


Copy number variation in the speciation of pigs: a possible prominent role for olfactory receptors.

Paudel Y, Madsen O, Megens HJ, Frantz LA, Bosse M, Crooijmans RP, Groenen MA - BMC Genomics (2015)

Simple schematic diagram of tested constrained models. A: Constrained model 1 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus celebensis. B: Constrained model 2 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus verrucosus. C: Constrained model 3 where other species consists of Sus scrofa (Europe and China) and Sus cebifrons, Sus celebensis and Sus verrucosus. D: Constrained model 4 where other species consists of Sus scrofa (Sumatra and Europe) and Sus barbatus, Sus celebensis and Sus verrucosus.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4413995&req=5

Fig5: Simple schematic diagram of tested constrained models. A: Constrained model 1 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus celebensis. B: Constrained model 2 where other species consists of Sus scrofa (Europe and China) and Sus barbatus, Sus cebifrons and Sus verrucosus. C: Constrained model 3 where other species consists of Sus scrofa (Europe and China) and Sus cebifrons, Sus celebensis and Sus verrucosus. D: Constrained model 4 where other species consists of Sus scrofa (Sumatra and Europe) and Sus barbatus, Sus celebensis and Sus verrucosus.
Mentions: To further evaluate the discrepancies between the different partitions we performed a more parametric phylogenetic approach, Bayesian phylogenetic analysis, using the MKV model [42] as implemented in MrBayes v2.2 [43], and an extending encoding of the CNs. We first ran the MKV model without any topology constrains and found that the monophyly of the Sus-ISEA and Sus scrofa clades, as identified by the SNP data and in previous analyses [31], was highly supported (posterior probability PP > 0.9) for both CNVR-OR and CNVR-ALL, but not for CNVR-nonOR which supported a Sus cebifons and Sus scrofa (China) relationship. To address the strength of support for these discrepancies we tested different constrained models that fit the history of inter-specific admixture [31]. We first computed the support (marginal likelihood; see methods) for a model in which the monophyly of Sus-ISEA and Sus scrofa clades were constrained, a scenario consistent with the SNP tree. Thereafter 4 different models were tested that are described in Figure 5 A-D. In Model-1, we constrained Sus verrucosus and Sus scrofa Sumatra to be monophyletic (Figure 5A), representing known admixture among these species [31]. In Model-2, we constrained Sus celebensis and Sus scrofa Sumatra to be monophyletic (Figure 5B) representing possible human translocations of Sus celebensis to Sumatra and neighboring islands. In Model-3, Sus barbatus and Sus scrofa Sumatra were constrained to be monophyletic (Figure 5C), representing known admixture between these two species/populations. In Model-4, Sus cebifrons and Sus scrofa China were constrained to be monophyletic (Figure 5D), representing possible migration from MSEA to the Philippines [31]. The marginal likelihood analysis strongly supports the monophyly of the two major clade of Sus-ISEA and Sus scrofa for CNVR-OR and CNVR-ALL but not for CNVR-nonOR where this monophyly provides a much poorer fit. For CNVR-nonOR the difference in marginal likelihood (delta-lnL) to the model was 7.46 (Table 2), which strongly supports the non-monophyly of the two major clades.Figure 5

Bottom Line: Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation.Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species.These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs).

View Article: PubMed Central - PubMed

Affiliation: Animal Breeding and Genomics Centre, Wageningen University, 6700 AH, Wageningen, The Netherlands. paudelyogesh@gmail.com.

ABSTRACT

Background: Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation. Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species. Previous studies provided detailed knowledge on the potential evolutionary role of SVs, especially copy number variations (CNVs), between well diverged species of e.g. primates. However, our understanding of their significance during ongoing speciation processes is limited due to the lack of CNV data from closely related species. The genus Sus (pig and its close relatives) which started to diverge ~4 Mya presents an excellent model for studying the role of CNVs during ongoing speciation.

Results: In this study, we identified 1408 CNV regions (CNVRs) across the genus Sus. These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs). The majority of these copy number variable genes are olfactory receptors (ORs) known to play a prominent role in food foraging and mate recognition in Sus. Phylogenetic analyses, including novel Bayesian analysis, based on CNVRs that overlap ORs retain the well-accepted topology of the genus Sus whereas CNVRs overlapping genes other than ORs show evidence for random drift and/or admixture.

Conclusion: We hypothesize that inter-specific variation in copy number of ORs provided the means for rapid adaptation to different environments during the diversification of the genus Sus in the Pliocene. Furthermore, these regions might have acted as barriers preventing massive gene flow between these species during the multiple hybridization events that took place later in the Pleistocene suggesting a possible prominent role of ORs in the ongoing Sus speciation.

No MeSH data available.