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Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria - PubMed

  • ️Thu Jan 01 2015

Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria

Sandra B Andersen et al. BMC Evol Biol. 2015.

Abstract

Background: The obligate mutualism between fungus-growing ants and microbial symbionts offers excellent opportunities to study the specificity and stability of multi-species interactions. In addition to cultivating fungus gardens, these ants have domesticated actinomycete bacteria to defend gardens against the fungal parasite Escovopsis and possibly other pathogens. Panamanian Acromyrmex echinatior leaf-cutting ants primarily associate with actinomycetes of the genus Pseudonocardia. Colonies are inoculated with one of two vertically transmitted phylotypes (Ps1 or Ps2), and maintain the same phylotype over their lifetime. We performed a cross-fostering experiment to test whether co-adaptations between ants and bacterial phylotypes have evolved, and how this affects bacterial growth and ant prophylactic behavior after infection with Escovopsis.

Results: We show that Pseudonocardia readily colonized ants irrespective of their colony of origin, but that the Ps2 phylotype, which was previously shown to be better able to maintain its monocultural integrity after workers became foragers than Ps1, reached a higher final cover when grown on its native host than on alternative hosts. The frequencies of major grooming and weeding behaviors co-varied with symbiont/host combinations, showing that ant behavior also was affected when cuticular actinomycete phylotypes were swapped.

Conclusion: These results show that the interactions between leaf-cutting ants and Pseudonocardia bear signatures of mutual co-adaptation within a single ant population.

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Figures

Figure 1
Figure 1

The cross-fostering experiment set-up. Fungus gardens and pupae from four source colonies were used to set up 32 subcolonies in a duplicated (4x4) fully crossed design. Source colony identity is indicated by color, with blue used for colonies with Pseudonocardia phylotype 1 (Ps1) and red/orange for colonies with Pseudonocardia phylotype 2 (Ps2). Pupae from each source colony eclosed in two replicate subcolonies with either a garden fragment and nurse workers from their own colony (e.g. light blue pupae in light blue garden), or a garden fragment and nurse workers from a colony with the same Pseudonocardia phylotype (e.g. light blue pupae in dark blue garden), or a garden fragment and nurse workers from two colonies with the other Pseudonocardia phylotype (e.g. light blue pupae in red and orange gardens). Drawing of pupae from

http://etc.usf.edu/clipart

.

Figure 2
Figure 2

Bacterial growth rates on ant cuticles. A. Boxplot of the bacterial cover scores of all individuals from all subcolonies from day 0 – 19 and 2 weeks after Escovopsis infection: Box-and-whisker plots, with the middle band representing the median, the bottom and top of the boxes representing the 25th and 75th percentiles, the lower and upper whiskers the 5% and 95% percentiles, and points beyond these shown as open circles. At day 0 all individuals had a score of 0. B. Bacterial cover scores with the solid lines showing the median cover and the dashed lines indicating the 25% and 75% percentiles for all individuals in the two replicate subcolonies for each treatment. For each plot the source colony of the fungus garden and the pupae is indicated, in addition to the identity of the native Pseudonocardia phylotype (colors as in figure 1). White background plots are crossings of the same phylotype inoculating ants of another colony having the same Pseudonocardia, and shaded plots are crossings where gardens/nurses and pupae were from colonies with a different Pseudonocardia phylotype.

Figure 3
Figure 3

The effect of Pseudonocardia phylotype combination (in subcolonies composed of pupae and gardens/nurses with Ps1 or Ps2 in all four combinations) on behavioral profiles, usually defined as principal components (A - E, see text for details) and final cover (F). Box plots are drawn as in figure 2A. A. PC1 capturing the negatively correlated behaviors self-grooming (positive values) and immobile in the fungus garden (negative values). Workers with their native phylotype spent more time self-grooming, although this was not statistically significant after Bonferroni correction. B. PC2 showing fungus-grooming. Workers with Ps2 as their native phylotype, marked with an *, spend significantly less time fungus-grooming in Ps2 gardens than all others. C. PC3 showing allo-grooming. Workers with Ps2 as their native phylotype, marked with an *, spend significantly more time allo-grooming than all others. D. PC4 showing garden-weeding. There were no significant differences between phylotypes or their combinations. E. Time spent outside the fungus garden. Workers with Ps2 as their native phylotype, marked with an *, spend significantly more time outside. In addition to this overall difference, when they were reared in a Ps1 garden they spent significantly less time outside compared to when reared in a Ps2 garden, marked with **, but still more than workers with Ps1 as their native phyloptype. F. Final bacterial cover of cross-fostered ants estimated two weeks after infection with Escovopsis. There was a significant effect of Pseudonocardia phylotype and an interaction between pupal phylotype and fungus garden phylotype, so workers with Ps2 as their native phylotype reached a higher cover, marked with an *, especially in Ps2 gardens, marked with **. The size of the data points indicate the frequency of the cover index.

Figure 4
Figure 4

Nine monitored behaviors expressed by tending large worker ants 15–19 days after eclosion following Escovopsis infection of their gardens, presented as mean proportions of time spent on each behavior ± SE. Plots are organized according to fostering treatments with garden phylotype followed by pupal phylotype (columns) and time since colonies were infected on Day 0 (rows). Self-grooming, fungus-grooming and allo-grooming were the most common behaviors, whereas garden-weeding was mainly observed on the day of infection (Day 0) and decreased significantly over the three days.

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References

    1. Herre EA, Knowlton N, Mueller UG, Rehner SA. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol. 1999;14:49–53. doi: 10.1016/S0169-5347(98)01529-8. - DOI - PubMed
    1. Queller DC, Strassmann JE. Beyond society: the evolution of organismality. Philos Trans R Soc B-Biological Sci. 2009;364:3143–55. doi: 10.1098/rstb.2009.0095. - DOI - PMC - PubMed
    1. Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science (80-) 2010;330:243–6. doi: 10.1126/science.1190333. - DOI - PMC - PubMed
    1. Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, et al. Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci U S A. 2010;107:17234–9. doi: 10.1073/pnas.1006872107. - DOI - PMC - PubMed
    1. De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, Wargo AR, et al. Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci U S A. 2005;102:7624–8. doi: 10.1073/pnas.0500078102. - DOI - PMC - PubMed

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