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High variability in a mating type linked region in the dry rot fungus Serpula lacrymans caused by frequency-dependent selection?

Engh IB, Skrede I, Saetre GP, Kauserud H - BMC Genet. (2010)

Bottom Line: High allelic richness and molecular variation was detected in the mating type linked marker as compared to other presumably neutral markers.The analyzed DNA marker displays trans-species polymorphism wherein some alleles from the closely related species S. himantoides are more similar to those of S. lacrymans than other alleles from S. himantoides.Our results support the idea that strong negative frequency-dependent selection maintains high levels of genetic variation in MAT-linked genomic regions, even in recently bottlenecked populations of S. lacrymans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Microbial Evolution Research Group, Department of Biology, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway.

ABSTRACT

Background: The mating type loci that govern the mating process in fungi are thought to be influenced by negative frequency-dependent selection due to rare allele advantage. In this study we used a mating type linked DNA marker as a proxy to indirectly study the allelic richness and geographic distribution of mating types of one mating type locus (MAT A) in worldwide populations of the dry rot fungus Serpula lacrymans. This fungus, which causes serious destruction to wooden constructions in temperate regions worldwide, has recently expanded its geographic range with a concomitant genetic bottleneck.

Results: High allelic richness and molecular variation was detected in the mating type linked marker as compared to other presumably neutral markers. Comparable amounts of genetic variation appeared in the mating type linked marker in populations from nature and buildings, which contrast the pattern observed with neutral genetic markers where natural populations were far more variable. Some geographic structuring of the allelic variation in the mating type linked marker appeared, but far less than that observed with neutral markers. In founder populations of S. lacrymans, alleles co-occurring in heterokaryotic individuals were more divergent than expected by chance, which agrees with the expectation for populations where few mating alleles exists. The analyzed DNA marker displays trans-species polymorphism wherein some alleles from the closely related species S. himantoides are more similar to those of S. lacrymans than other alleles from S. himantoides.

Conclusions: Our results support the idea that strong negative frequency-dependent selection maintains high levels of genetic variation in MAT-linked genomic regions, even in recently bottlenecked populations of S. lacrymans.

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Related in: MedlinePlus

Phylogenies of the MAT A linked marker and ITS. 50% majority rule consensus trees obtained from Bayesian analyses of (a) the MAT A linked marker data sets, and (b) the ITS region. In both datasets DNA sequences were obtained from 83 isolates representing S. lacrymans and S. himantioides. Bayesian posterior probabilities above 0.50 are given above branches and Jackknife support values (1000 replicates) above 50 are given below branches. The tree symbols indicate isolates derived from a natural habitat (forest), otherwise the isolates were obtained from buildings. The star symbols indicate isolates with more than two alleles of the mating type linked marker while the arrows pinpoints trans-specific polymorphisms.
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Figure 1: Phylogenies of the MAT A linked marker and ITS. 50% majority rule consensus trees obtained from Bayesian analyses of (a) the MAT A linked marker data sets, and (b) the ITS region. In both datasets DNA sequences were obtained from 83 isolates representing S. lacrymans and S. himantioides. Bayesian posterior probabilities above 0.50 are given above branches and Jackknife support values (1000 replicates) above 50 are given below branches. The tree symbols indicate isolates derived from a natural habitat (forest), otherwise the isolates were obtained from buildings. The star symbols indicate isolates with more than two alleles of the mating type linked marker while the arrows pinpoints trans-specific polymorphisms.

Mentions: We found higher molecular variation in the mating type linked marker compared to the other sequenced loci (Table 1). Fig. 1 shows higher allelic variation in the mating type linked marker than in the ITS region. In the phylogenetic tree obtained from the mating type linked marker, the samples of var. lacrymans from Europe, North-America and Oceania (i.e. the 'Cosmopolitan group' [12], and the Japanese population appeared to a large extent intermixed on several branches. This is in contrast to the ITS tree (Fig. 1), as well as trees based on other analysed markers [12] where the Japanese and Cosmopolitan samples appear in two quite distinct groups. Furthermore, a comparable amount of genetic variation appeared in the mating type linked marker in populations of S. lacrymans from nature and buildings. This is in stark contrast to the pattern observed using neutral genetic markers, where natural populations were far more genetically variable than those from buildings (Table 1). The high level of genetic variation at the mating type linked marker compared to the presumably neutrally evolving markers may be explained by negative frequency-dependent selection at the MAT A locus maintaining genetic variation also in the vicinity of the locus under selection. In accordance with this hypothesis the results from the HKA test showed that there was significant deviation from neutral evolution when we compared the mating type linked marker with the presumably neutral markers ITS, tub or gpd. This test was based on intra- and interspecific divergence within and between S. lacrymans var. shastensis and var. lacrymans. Balancing selection, such as negative frequency-dependent selection, will often tend to keep alleles at intermediate frequencies. Accordingly, rare alleles will tend to be underrepresented compared to neutral expectation. Thus neutrality tests, such as Tajima's D will often yield positive test statistics at such loci. In contrast, the test statistics of Tajima's D, Fu and Li's D (Table 1) were negative at the mating type linked marker in the populations investigated here. In a previous study we found strong signals for a recent population expansion in these fungi [12], a demographic process that usually would affect the test-statistics of these neutrality tests in the opposite direction compared to balancing selection. Hence, we suggest that demographic effects may override the expected signal from balancing selection in this case.


High variability in a mating type linked region in the dry rot fungus Serpula lacrymans caused by frequency-dependent selection?

Engh IB, Skrede I, Saetre GP, Kauserud H - BMC Genet. (2010)

Phylogenies of the MAT A linked marker and ITS. 50% majority rule consensus trees obtained from Bayesian analyses of (a) the MAT A linked marker data sets, and (b) the ITS region. In both datasets DNA sequences were obtained from 83 isolates representing S. lacrymans and S. himantioides. Bayesian posterior probabilities above 0.50 are given above branches and Jackknife support values (1000 replicates) above 50 are given below branches. The tree symbols indicate isolates derived from a natural habitat (forest), otherwise the isolates were obtained from buildings. The star symbols indicate isolates with more than two alleles of the mating type linked marker while the arrows pinpoints trans-specific polymorphisms.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2909151&req=5

Figure 1: Phylogenies of the MAT A linked marker and ITS. 50% majority rule consensus trees obtained from Bayesian analyses of (a) the MAT A linked marker data sets, and (b) the ITS region. In both datasets DNA sequences were obtained from 83 isolates representing S. lacrymans and S. himantioides. Bayesian posterior probabilities above 0.50 are given above branches and Jackknife support values (1000 replicates) above 50 are given below branches. The tree symbols indicate isolates derived from a natural habitat (forest), otherwise the isolates were obtained from buildings. The star symbols indicate isolates with more than two alleles of the mating type linked marker while the arrows pinpoints trans-specific polymorphisms.
Mentions: We found higher molecular variation in the mating type linked marker compared to the other sequenced loci (Table 1). Fig. 1 shows higher allelic variation in the mating type linked marker than in the ITS region. In the phylogenetic tree obtained from the mating type linked marker, the samples of var. lacrymans from Europe, North-America and Oceania (i.e. the 'Cosmopolitan group' [12], and the Japanese population appeared to a large extent intermixed on several branches. This is in contrast to the ITS tree (Fig. 1), as well as trees based on other analysed markers [12] where the Japanese and Cosmopolitan samples appear in two quite distinct groups. Furthermore, a comparable amount of genetic variation appeared in the mating type linked marker in populations of S. lacrymans from nature and buildings. This is in stark contrast to the pattern observed using neutral genetic markers, where natural populations were far more genetically variable than those from buildings (Table 1). The high level of genetic variation at the mating type linked marker compared to the presumably neutrally evolving markers may be explained by negative frequency-dependent selection at the MAT A locus maintaining genetic variation also in the vicinity of the locus under selection. In accordance with this hypothesis the results from the HKA test showed that there was significant deviation from neutral evolution when we compared the mating type linked marker with the presumably neutral markers ITS, tub or gpd. This test was based on intra- and interspecific divergence within and between S. lacrymans var. shastensis and var. lacrymans. Balancing selection, such as negative frequency-dependent selection, will often tend to keep alleles at intermediate frequencies. Accordingly, rare alleles will tend to be underrepresented compared to neutral expectation. Thus neutrality tests, such as Tajima's D will often yield positive test statistics at such loci. In contrast, the test statistics of Tajima's D, Fu and Li's D (Table 1) were negative at the mating type linked marker in the populations investigated here. In a previous study we found strong signals for a recent population expansion in these fungi [12], a demographic process that usually would affect the test-statistics of these neutrality tests in the opposite direction compared to balancing selection. Hence, we suggest that demographic effects may override the expected signal from balancing selection in this case.

Bottom Line: High allelic richness and molecular variation was detected in the mating type linked marker as compared to other presumably neutral markers.The analyzed DNA marker displays trans-species polymorphism wherein some alleles from the closely related species S. himantoides are more similar to those of S. lacrymans than other alleles from S. himantoides.Our results support the idea that strong negative frequency-dependent selection maintains high levels of genetic variation in MAT-linked genomic regions, even in recently bottlenecked populations of S. lacrymans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Microbial Evolution Research Group, Department of Biology, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway.

ABSTRACT

Background: The mating type loci that govern the mating process in fungi are thought to be influenced by negative frequency-dependent selection due to rare allele advantage. In this study we used a mating type linked DNA marker as a proxy to indirectly study the allelic richness and geographic distribution of mating types of one mating type locus (MAT A) in worldwide populations of the dry rot fungus Serpula lacrymans. This fungus, which causes serious destruction to wooden constructions in temperate regions worldwide, has recently expanded its geographic range with a concomitant genetic bottleneck.

Results: High allelic richness and molecular variation was detected in the mating type linked marker as compared to other presumably neutral markers. Comparable amounts of genetic variation appeared in the mating type linked marker in populations from nature and buildings, which contrast the pattern observed with neutral genetic markers where natural populations were far more variable. Some geographic structuring of the allelic variation in the mating type linked marker appeared, but far less than that observed with neutral markers. In founder populations of S. lacrymans, alleles co-occurring in heterokaryotic individuals were more divergent than expected by chance, which agrees with the expectation for populations where few mating alleles exists. The analyzed DNA marker displays trans-species polymorphism wherein some alleles from the closely related species S. himantoides are more similar to those of S. lacrymans than other alleles from S. himantoides.

Conclusions: Our results support the idea that strong negative frequency-dependent selection maintains high levels of genetic variation in MAT-linked genomic regions, even in recently bottlenecked populations of S. lacrymans.

Show MeSH
Related in: MedlinePlus