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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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A representation of the circular genome ofA. phagocytophilumbased on the sequenced HZ strain (NC_007797.1, [23]). The outer circle (orange & purple) gives genome landmarks in base pairs. The two purple sections indicate the locations of two p44 pseudogene clusters [65]. The inner circle (dark blue) shows the location of the seven genetic regions used in this study (pink bars) as well as six other genetic regions that have been important for A. phagocytophilum strain characterization or may have functional importance in host interactions (light blue bars). Green arrows indicate that the coding sequence of a genetic region is in the forward direction relative to the published genome and red arrows indicate that the coding sequence of the genetic region is in the reverse direction relative to the published genome. (See Additional file 1: Table S5 for more details).
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Fig3: A representation of the circular genome ofA. phagocytophilumbased on the sequenced HZ strain (NC_007797.1, [23]). The outer circle (orange & purple) gives genome landmarks in base pairs. The two purple sections indicate the locations of two p44 pseudogene clusters [65]. The inner circle (dark blue) shows the location of the seven genetic regions used in this study (pink bars) as well as six other genetic regions that have been important for A. phagocytophilum strain characterization or may have functional importance in host interactions (light blue bars). Green arrows indicate that the coding sequence of a genetic region is in the forward direction relative to the published genome and red arrows indicate that the coding sequence of the genetic region is in the reverse direction relative to the published genome. (See Additional file 1: Table S5 for more details).

Mentions: The differences in the amount of standing genetic diversity observed within the three A. phagocytophilum strains suggest that selection and/or demography has differed between them. In recombining organisms the effects of selection are expected to occur locally, whereas the effects of demographic change should be observable genome wide. However, in clonal organisms such as bacteria, selection will affect diversity across the entire genome unless recombination breaks up linkages between genomic regions [24]. While such recombination was once considered rare in bacteria, increasing evidence suggests that it can occur at a sufficient rate to minimize linkages among loci [25,26]. The seven genetic regions in this study are distributed broadly across the A. phagocytophilum genome, making it possible that they have evolved at least semi-independently (FigureĀ 3). Furthermore, homologous recombination plays a large roll in allowing A. phagocytophilum populations to avoid immune defenses and adapt to specific hosts [27]. This may also reduce the influence of linkage on genetic diversity patterns in this bacterium.Figure 3


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)

A representation of the circular genome ofA. phagocytophilumbased on the sequenced HZ strain (NC_007797.1, [23]). The outer circle (orange & purple) gives genome landmarks in base pairs. The two purple sections indicate the locations of two p44 pseudogene clusters [65]. The inner circle (dark blue) shows the location of the seven genetic regions used in this study (pink bars) as well as six other genetic regions that have been important for A. phagocytophilum strain characterization or may have functional importance in host interactions (light blue bars). Green arrows indicate that the coding sequence of a genetic region is in the forward direction relative to the published genome and red arrows indicate that the coding sequence of the genetic region is in the reverse direction relative to the published genome. (See Additional file 1: Table S5 for more details).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: A representation of the circular genome ofA. phagocytophilumbased on the sequenced HZ strain (NC_007797.1, [23]). The outer circle (orange & purple) gives genome landmarks in base pairs. The two purple sections indicate the locations of two p44 pseudogene clusters [65]. The inner circle (dark blue) shows the location of the seven genetic regions used in this study (pink bars) as well as six other genetic regions that have been important for A. phagocytophilum strain characterization or may have functional importance in host interactions (light blue bars). Green arrows indicate that the coding sequence of a genetic region is in the forward direction relative to the published genome and red arrows indicate that the coding sequence of the genetic region is in the reverse direction relative to the published genome. (See Additional file 1: Table S5 for more details).
Mentions: The differences in the amount of standing genetic diversity observed within the three A. phagocytophilum strains suggest that selection and/or demography has differed between them. In recombining organisms the effects of selection are expected to occur locally, whereas the effects of demographic change should be observable genome wide. However, in clonal organisms such as bacteria, selection will affect diversity across the entire genome unless recombination breaks up linkages between genomic regions [24]. While such recombination was once considered rare in bacteria, increasing evidence suggests that it can occur at a sufficient rate to minimize linkages among loci [25,26]. The seven genetic regions in this study are distributed broadly across the A. phagocytophilum genome, making it possible that they have evolved at least semi-independently (FigureĀ 3). Furthermore, homologous recombination plays a large roll in allowing A. phagocytophilum populations to avoid immune defenses and adapt to specific hosts [27]. This may also reduce the influence of linkage on genetic diversity patterns in this bacterium.Figure 3

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