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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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Phylogeny of the threeA. phagocytophilumstrains used in this study based on seven conserved genetic regions. Rather than display each branch tip individually we have chosen to represent each of the three clusters with a composite triangle. The vertical height of the triangle indicates relative sample sizes for each strain examined in this study. The horizontal width of the triangle indicates the extent of intra-strain synonymous genetic diversity. The numbers along each branch indicate the observed number of synonymous substitutions per synonymous site (dS). The vertical order of the taxa displayed within each cluster is arbitrary.
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Fig1: Phylogeny of the threeA. phagocytophilumstrains used in this study based on seven conserved genetic regions. Rather than display each branch tip individually we have chosen to represent each of the three clusters with a composite triangle. The vertical height of the triangle indicates relative sample sizes for each strain examined in this study. The horizontal width of the triangle indicates the extent of intra-strain synonymous genetic diversity. The numbers along each branch indicate the observed number of synonymous substitutions per synonymous site (dS). The vertical order of the taxa displayed within each cluster is arbitrary.

Mentions: To examine the influence of host range variation on effective population size and intra-specific evolutionary divergence, we examined genetic diversity among distinct populations of the obligately intercellular bacterium Anaplasma phagocytophilum. As a bacterial species, this emerging zoonotic pathogen infects a broad range of vertebrate hosts [4]. However, there are multiple, discrete strains of A. phagocytophilum circulating in Europe, with minimal overlap in their host associations [13-15]. One of these strains is a generalist with a relatively broad host range, encompassing mammal species from a wide taxonomic spectrum (Figure 1). This is also the strain that overwhelmingly infects humans, livestock and other domestic animals [13-15]. By contrast, a second strain appears to specialize almost exclusively on roe deer. Both of these strains share the same primary tick vector, Ixodes ricinus. A third strain of mammal-infecting A. phagocytophilum is also circulating in Europe, but it is unclear whether this population can be classified as either a specialist or generalist. It predominately infects small mammals such as voles and shrews. This strain’s ecologically narrow host range is due in part to transmission by the nest-living tick species Ixodes trianguliceps [13]. However, while its potential hosts may share many ecological similarities, rodents and insectivores are among the most evolutionary divergent mammals capable of harboring A. phagocytophilum. Each belongs to a distinct superorder and their respective lineages diverged between 74 and 98 million years ago [16]. Immunity and other factors affecting bacterial population growth may differ greatly between these hosts [17], which likely constrains the ability of A. phagocytophilum to adapt to these species.Figure 1


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)

Phylogeny of the threeA. phagocytophilumstrains used in this study based on seven conserved genetic regions. Rather than display each branch tip individually we have chosen to represent each of the three clusters with a composite triangle. The vertical height of the triangle indicates relative sample sizes for each strain examined in this study. The horizontal width of the triangle indicates the extent of intra-strain synonymous genetic diversity. The numbers along each branch indicate the observed number of synonymous substitutions per synonymous site (dS). The vertical order of the taxa displayed within each cluster is arbitrary.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Phylogeny of the threeA. phagocytophilumstrains used in this study based on seven conserved genetic regions. Rather than display each branch tip individually we have chosen to represent each of the three clusters with a composite triangle. The vertical height of the triangle indicates relative sample sizes for each strain examined in this study. The horizontal width of the triangle indicates the extent of intra-strain synonymous genetic diversity. The numbers along each branch indicate the observed number of synonymous substitutions per synonymous site (dS). The vertical order of the taxa displayed within each cluster is arbitrary.
Mentions: To examine the influence of host range variation on effective population size and intra-specific evolutionary divergence, we examined genetic diversity among distinct populations of the obligately intercellular bacterium Anaplasma phagocytophilum. As a bacterial species, this emerging zoonotic pathogen infects a broad range of vertebrate hosts [4]. However, there are multiple, discrete strains of A. phagocytophilum circulating in Europe, with minimal overlap in their host associations [13-15]. One of these strains is a generalist with a relatively broad host range, encompassing mammal species from a wide taxonomic spectrum (Figure 1). This is also the strain that overwhelmingly infects humans, livestock and other domestic animals [13-15]. By contrast, a second strain appears to specialize almost exclusively on roe deer. Both of these strains share the same primary tick vector, Ixodes ricinus. A third strain of mammal-infecting A. phagocytophilum is also circulating in Europe, but it is unclear whether this population can be classified as either a specialist or generalist. It predominately infects small mammals such as voles and shrews. This strain’s ecologically narrow host range is due in part to transmission by the nest-living tick species Ixodes trianguliceps [13]. However, while its potential hosts may share many ecological similarities, rodents and insectivores are among the most evolutionary divergent mammals capable of harboring A. phagocytophilum. Each belongs to a distinct superorder and their respective lineages diverged between 74 and 98 million years ago [16]. Immunity and other factors affecting bacterial population growth may differ greatly between these hosts [17], which likely constrains the ability of A. phagocytophilum to adapt to these species.Figure 1

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