Contrasting patterns in mammal-bacteria coevolution: bartonella and leptospira in bats and rodents

Abstract

Background: Emerging bacterial zoonoses in bats and rodents remain relatively understudied. We conduct the first comparative host-pathogen coevolutionary analyses of bacterial pathogens in these hosts, using Bartonella spp. and Leptospira spp. as a model.

Methodology/principal findings: We used published genetic data for 51 Bartonella genotypes from 24 bat species, 129 Bartonella from 38 rodents, and 26 Leptospira from 20 bats. We generated maximum likelihood and Bayesian phylogenies for hosts and bacteria, and tested for coevoutionary congruence using programs ParaFit, PACO, and Jane. Bartonella spp. and their bat hosts had a significant coevolutionary fit (ParaFitGlobal = 1.9703, P≤0.001; m2 global value = 7.3320, P≤0.0001). Bartonella spp. and rodent hosts also indicated strong overall patterns of cospeciation (ParaFitGlobal = 102.4409, P≤0.001; m2 global value = 86.532, P≤0.0001). In contrast, we were unable to reject independence of speciation events in Leptospira and bats (ParaFitGlobal = 0.0042, P = 0.84; m2 global value = 4.6310, P = 0.5629). Separate analyses of New World and Old World data subsets yielded results congruent with analysis from entire datasets. We also conducted event-based cophylogeny analyses to reconstruct likely evolutionary histories for each group of pathogens and hosts. Leptospira and bats had the greatest number of host switches per parasite (0.731), while Bartonella and rodents had the fewest (0.264).

Conclusions/significance: In both bat and rodent hosts, Bartonella exhibits significant coevolution with minimal host switching, while Leptospira in bats lacks evolutionary congruence with its host and has high number of host switches. Reasons underlying these variable coevolutionary patterns in host range are likely due to differences in disease-specific transmission and host ecology. Understanding the coevolutionary patterns and frequency of host-switching events between bacterial pathogens and their hosts will allow better prediction of spillover between mammal reservoirs, and ultimately to humans.

Figure 1. Tanglegram of cophylogenetic relationships between New World bat hosts and Bartonella.

Maximum likelihood phylogenies for Bartonella bacteria (yellow) and their New World bat hosts (blue), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as gray and black connecting lines. Black lines indicate significant individual cospeciation links between Bartonella and their hosts as indicated by ParaFit (P≤0.05), while gray lines represent non-significant links. Bat species that did not have an available cytochrome b sequence on GenBank, is substituted with a closely related species. Phyllostomus hastatus substituted for Phyllostomus discolor.

Figure 2. Tanglegram of cophylogenetic relationships between Old World bat hosts and Bartonella.

Maximum likelihood phylogenies for Bartonella bacteria (yellow) and their Old World bat hosts (blue), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as gray and black connecting lines. Black lines indicate significant individual cospeciation links between Bartonella and their hosts as indicated by ParaFit (P≤0.05), while gray lines are non-significant links. Bat species that did not have an available cytochrome b sequence on GenBank, is substituted with a closely related species. Triaenops persicus substituted for Triaenops menamena, and Hipposideros armiger for Hipposideros commersoni.

Figure 3. Tanglegram of cophylogenetic relationships between New World rodent hosts and Bartonella.

Maximum likelihood phylogenies for Bartonella bacteria (yellow) and their New World rodent hosts (green), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as black connecting lines and are significant as indicated by ParaFit (P≤0.05).

Figure 4. Tanglegram of cophylogenetic relationships between Old World rodent hosts and Bartonella.

Maximum likelihood phylogenies for Bartonella bacteria (yellow) and their Old World rodent hosts (green), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as gray and black connecting lines. Black lines indicate significant individual cospeciation links between Bartonella and their hosts as indicated by ParaFit (P≤0.05), while gray lines are non-significant links.

Figure 5. Tanglegram of cophylogenetic relationships between New World bat hosts and Leptospira.

Maximum likelihood phylogenies for Leptospira bacteria (pink) and their New World bat hosts (blue), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as gray connecting lines, and are insignificant as indicated by ParaFit (P≤0.05). Bat species that did not have an available cytochrome b sequence on GenBank, is substituted with a closely related species. Phyllostomus hastatus substituted for Phyllostomus discolor, Promops centralis for Promops nasutus.

Figure 6. Tanglegram of cophylogenetic relationships between Old World bat hosts and Leptospira.

Maximum likelihood phylogenies for Leptospira bacteria (pink) and their Old World bat hosts (blue), with bootstrap support values ≥50 labeled, rooted with outgroups. All host-pathogen associations are shown in the tanglegram as gray connecting lines, and are significant as indicated by ParaFit (P≤0.05). Bat species that did not have an available cytochrome b sequence on GenBank, is substituted with a closely related species. Triaenops persicus substituted for Triaenops menamena.