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Varying influences of selection and demography in host-adapted populations of the tick-transmitted bacterium, Anaplasma phagocytophilum.

Aardema ML, von Loewenich FD - BMC Evol. Biol. (2015)

Bottom Line: Strains of A. phagocytophilum display varying degrees of host specialization, making this a good species for exploring questions regarding host range, effective population size and selection efficacy.We found that a roe deer specialist harbored the most genetic diversity of the three A. phagocytophilum strains and correspondingly had the largest effective population size.A. phagocytophilum is a diverse bacterial species that differs among distinct strains in its effective population size, as well as how genetic diversity and divergence have been influenced by selection and demographic changes.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA. maardema@princeton.edu.

ABSTRACT

Background: The host range of a pathogenic bacterial strain likely influences its effective population size, which in turn affects the efficacy of selection. Transmission between competent hosts may occur more frequently for host generalists than for specialists. This could allow higher bacterial population densities to persist within an ecological community and increase the efficacy of selection in these populations. Conversely, specialist strains may be better adapted to their hosts and consequently achieve greater within-host population densities, with corresponding increases in selection efficacy. To assess these different hypotheses, we examined the effective population sizes of three strains of the bacterium Anaplasma phagocytophilum and categorized the varying roles of selection and demography on patterns of genetic diversity and divergence in these populations. A. phagocytophilum is a tick-transmitted, obligately intracellular pathogen. Strains of A. phagocytophilum display varying degrees of host specialization, making this a good species for exploring questions regarding host range, effective population size and selection efficacy.

Results: We found that a roe deer specialist harbored the most genetic diversity of the three A. phagocytophilum strains and correspondingly had the largest effective population size. Another strain that is ecologically specialized on rodents and insectivores had the smallest effective population size. However, these mammalian hosts are distantly related evolutionarily. The third strain, a host generalist, was intermediate in its effective population size between the other two strains. Evolutionary constraint on non-synonymous sites was pervasive in all three strains, although some slightly deleterious mutations may also be segregating in these populations. We additionally found evidence of genome-wide selective sweeps in the generalist strain, whereas signals of repeated bottlenecks were detected in the strain with the smallest effective population size.

Conclusions: A. phagocytophilum is a diverse bacterial species that differs among distinct strains in its effective population size, as well as how genetic diversity and divergence have been influenced by selection and demographic changes. In this species, host specialization may facilitate increased population growth and allow more opportunities for selection to act. These results provide insights into how host range has influenced evolutionary patterns of strain divergence in an emerging zoonotic bacterium.

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Boxplots showing the median values (thick horizontal black lines) and quartiles for π (a & b) and θw(c & d) estimates at synonymous and non-synonymous sites. Open dots indicate outlying estimates. The red lines with asterisks indicate significant differences between clusters based on a paired t-test (p < 0.05). Note that for both synonymous π and θw the y-axis is on a Log10 scale.
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Fig2: Boxplots showing the median values (thick horizontal black lines) and quartiles for π (a & b) and θw(c & d) estimates at synonymous and non-synonymous sites. Open dots indicate outlying estimates. The red lines with asterisks indicate significant differences between clusters based on a paired t-test (p < 0.05). Note that for both synonymous π and θw the y-axis is on a Log10 scale.

Mentions: In agreement with our second hypothesis, we found that on average the cluster 2 strain harbored more pairwise genetic diversity than either clusters 1 or 3 (Figure 2a-d, Table 1, Additional file 1: Table S1). For non-synonymous π estimates, differences between strains were not significant (paired t tests, 1 vs. 2: t6 = -1.640, p = 0.152; 1 vs. 3: t6 = 0.057, p = 0.956; 2 vs. 3: t6 = 1.240, p = 0.261). For synonymous diversity, cluster 1 was significantly different from cluster 3 (paired t test, t6 = 3.074, p = 0.022), but despite having a higher average diversity level, cluster 2 was not significantly different from cluster 3 (paired t test, t6 = 1.928, p = 0.102). This is likely due to the high amount of variance in π estimates observed between loci in cluster 2 (Figure 2a, Table 1). Clusters 2 and 3 were also not significantly different from one another for synonymous π (paired t tests, t6 = -1.39, p = 0.213). Both clusters 1 and 2 were significantly different from cluster 3 for both synonymous and non-synonymous estimates of θW (paired t tests, synonymous θW: 1 vs 3: t6 = 5.219, p = 0.002; 2 vs 3: t6 = 2.549, p = 0.044; non-synonymous θW: 1 vs 3: t6 = 3.762, p = 0.009; 2 vs 3: t6 = 2.545, p = 0.044). However, they were not significantly different from each another (paired t tests, synonymous θW: 1 vs 2: t6 = -1.366, p = 0.221; non-synonymous θW: 1 vs 2: t6 = 0.698, p = 0.511).Figure 2


Varying influences of selection and demography in host-adapted populations of the tick-transmitted bacterium, Anaplasma phagocytophilum.

Aardema ML, von Loewenich FD - BMC Evol. Biol. (2015)

Boxplots showing the median values (thick horizontal black lines) and quartiles for π (a & b) and θw(c & d) estimates at synonymous and non-synonymous sites. Open dots indicate outlying estimates. The red lines with asterisks indicate significant differences between clusters based on a paired t-test (p < 0.05). Note that for both synonymous π and θw the y-axis is on a Log10 scale.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4383208&req=5

Fig2: Boxplots showing the median values (thick horizontal black lines) and quartiles for π (a & b) and θw(c & d) estimates at synonymous and non-synonymous sites. Open dots indicate outlying estimates. The red lines with asterisks indicate significant differences between clusters based on a paired t-test (p < 0.05). Note that for both synonymous π and θw the y-axis is on a Log10 scale.
Mentions: In agreement with our second hypothesis, we found that on average the cluster 2 strain harbored more pairwise genetic diversity than either clusters 1 or 3 (Figure 2a-d, Table 1, Additional file 1: Table S1). For non-synonymous π estimates, differences between strains were not significant (paired t tests, 1 vs. 2: t6 = -1.640, p = 0.152; 1 vs. 3: t6 = 0.057, p = 0.956; 2 vs. 3: t6 = 1.240, p = 0.261). For synonymous diversity, cluster 1 was significantly different from cluster 3 (paired t test, t6 = 3.074, p = 0.022), but despite having a higher average diversity level, cluster 2 was not significantly different from cluster 3 (paired t test, t6 = 1.928, p = 0.102). This is likely due to the high amount of variance in π estimates observed between loci in cluster 2 (Figure 2a, Table 1). Clusters 2 and 3 were also not significantly different from one another for synonymous π (paired t tests, t6 = -1.39, p = 0.213). Both clusters 1 and 2 were significantly different from cluster 3 for both synonymous and non-synonymous estimates of θW (paired t tests, synonymous θW: 1 vs 3: t6 = 5.219, p = 0.002; 2 vs 3: t6 = 2.549, p = 0.044; non-synonymous θW: 1 vs 3: t6 = 3.762, p = 0.009; 2 vs 3: t6 = 2.545, p = 0.044). However, they were not significantly different from each another (paired t tests, synonymous θW: 1 vs 2: t6 = -1.366, p = 0.221; non-synonymous θW: 1 vs 2: t6 = 0.698, p = 0.511).Figure 2

Bottom Line: Strains of A. phagocytophilum display varying degrees of host specialization, making this a good species for exploring questions regarding host range, effective population size and selection efficacy.We found that a roe deer specialist harbored the most genetic diversity of the three A. phagocytophilum strains and correspondingly had the largest effective population size.A. phagocytophilum is a diverse bacterial species that differs among distinct strains in its effective population size, as well as how genetic diversity and divergence have been influenced by selection and demographic changes.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA. maardema@princeton.edu.

ABSTRACT

Background: The host range of a pathogenic bacterial strain likely influences its effective population size, which in turn affects the efficacy of selection. Transmission between competent hosts may occur more frequently for host generalists than for specialists. This could allow higher bacterial population densities to persist within an ecological community and increase the efficacy of selection in these populations. Conversely, specialist strains may be better adapted to their hosts and consequently achieve greater within-host population densities, with corresponding increases in selection efficacy. To assess these different hypotheses, we examined the effective population sizes of three strains of the bacterium Anaplasma phagocytophilum and categorized the varying roles of selection and demography on patterns of genetic diversity and divergence in these populations. A. phagocytophilum is a tick-transmitted, obligately intracellular pathogen. Strains of A. phagocytophilum display varying degrees of host specialization, making this a good species for exploring questions regarding host range, effective population size and selection efficacy.

Results: We found that a roe deer specialist harbored the most genetic diversity of the three A. phagocytophilum strains and correspondingly had the largest effective population size. Another strain that is ecologically specialized on rodents and insectivores had the smallest effective population size. However, these mammalian hosts are distantly related evolutionarily. The third strain, a host generalist, was intermediate in its effective population size between the other two strains. Evolutionary constraint on non-synonymous sites was pervasive in all three strains, although some slightly deleterious mutations may also be segregating in these populations. We additionally found evidence of genome-wide selective sweeps in the generalist strain, whereas signals of repeated bottlenecks were detected in the strain with the smallest effective population size.

Conclusions: A. phagocytophilum is a diverse bacterial species that differs among distinct strains in its effective population size, as well as how genetic diversity and divergence have been influenced by selection and demographic changes. In this species, host specialization may facilitate increased population growth and allow more opportunities for selection to act. These results provide insights into how host range has influenced evolutionary patterns of strain divergence in an emerging zoonotic bacterium.

Show MeSH
Related in: MedlinePlus