Parallel Patterns of Increased Virulence in a Recently Emerged Wildlife Pathogen

Hawley, Dana M.; Osnas, Erik E.; Dobson, Andrew; Hochachka, Wesley M.; Ley, David; Dhondt, André A.

doi:10.1371/journal.pbio.1001570

Cited by 86 publications

(148 citation statements)

References 75 publications

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“…gallisepticum virulence for house finches has previously been shown to increase over time in a given geographic region (18). Data presented here confirm previous findings in that a recent HFMG isolate, VA2013, continues to be highly virulent in house finches.…”

Section: Discussionsupporting

confidence: 88%

“…Previous studies have shown that HFMG virulence evolution is not constant but is instead dynamic and dependent on ecological context (e.g., expanding versus established geographic ranges) (18,24). It is clear that M. gallisepticum was virulent for finches by the time that it was first noted and collected as VA1994 (coalescence analysis has indicated that HFMG first truly emerged in house finches 4 to 7 years prior [20,21]); however, here it is indicated that the period of time in which HFMG was circulating in finches prior to 1994 was insufficient to dramatically attenuate HFMG virulence for chickens.…”

Section: Discussionmentioning

confidence: 99%

“…These differences have indicated a decrease in HFMG virulence during transmission from eastern to western range hosts and parallel increases in HFMG virulence during local spread within eastern and western range host populations (17)(18)(19). Genomic changes occurring in the HFMG strain during the epidemic have been examined, again matching geotemporal patterns of isolation with phylogeny (20,21), and with the most dramatic genomic changes involving regions encoding phase-variable, surface-expressed lipoprotein (21).…”

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confidence: 99%

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Attenuated Phenotype of a Recent House Finch-Associated Mycoplasma gallisepticum Isolate in Domestic Poultry

et al. 2017

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Mycoplasma gallisepticum, known primarily as a respiratory pathogen of domestic poultry, has emerged since 1994 as a significant pathogen of the house finch (Haemorhous mexicanus) causing severe conjunctivitis and mortality. House finch-associated M. gallisepticum (HFMG) spread rapidly and increased in virulence for the finch host in the eastern United States. In the current study, we assessed virulence in domestic poultry with two temporally distant, and yet geographically consistent, HFMG isolates which differ in virulence for house finches-Virginia 1994 (VA1994), the index isolate of the epidemic, and Virginia 2013 (VA2013), a recent isolate of increased house finch virulence. Here we report a significant difference between VA1994 and VA2013 in their levels of virulence for chickens; notably, this difference correlated inversely to the difference in their levels of virulence for house finches. VA1994, while moderately virulent in house finches, displayed significant virulence in the chicken respiratory tract. VA2013, while highly virulent in the house finch, was significantly attenuated in chickens relative to VA1994, displaying lesssevere pathological lesions in, and reduced bacterial recovery from, the respiratory tract. Overall, these data indicate that a recent isolate of HFMG is greatly attenuated in the chicken host relative to the index isolate, notably demonstrating a virulence phenotype in chickens inversely related to that in the finch host.KEYWORDS Mycoplasma gallisepticum, chicken, house finch, pathology, virulence M ycoplasma gallisepticum is a bacterial pathogen associated with acute and chronic respiratory disease in domestic poultry. Previously, M. gallisepticum was thought to be relatively host specific and pathogenic only for gallinaceous birds (1). The emergence of M. gallisepticum infection in a wild North American songbird host-the house finch (Haemorhous mexicanus)-was first reported in 1994 in Virginia and Maryland and was associated with severe and chronic lymphoplasmacytic conjunctivitis, sinusitis, and rhinitis, contrasting with the respiratory form of M. gallisepticum disease primarily observed in poultry (2-4). The epidemic quickly spread throughout the eastern, or introduced, house finch range across the mid-Atlantic and the eastern states, and it eventually spread to the native house finch range in the western United States (2,(5)(6)(7)(8). House finch-associated M. gallisepticum (HFMG) has been associated with dramatic declines in house finch populations, likely as a result of affecting the host's ability to forage or to avoid predation (3,(9)(10)(11). This well-documented spread of HFMG has enabled dynamic modeling of various aspects of the epidemic as an example of the spread of an emergent pathogen (12, 13).

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Attenuated Phenotype of a Recent House Finch-Associated Mycoplasma gallisepticum Isolate in Domestic Poultry

et al. 2017

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“…We have contrasted virulence of a small number of isolates taken from different time periods, and from the eastern and western United States [25 -27]. These experiments suggest that parallel increases in virulence of the bacteria have occurred in both eastern and western North America over time, with the western increase following a lower initial virulence of the bacteria upon emergence on the Pacific coast [27]. These conclusions are valid to the extent that the small number of isolates used in these experiments [25 -27] are typical of the bacterial lineages circulating at the times and places where these isolates were collected.…”

Section: Resultsmentioning

confidence: 99%

Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen

et al. 2013

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Emergence of a new disease in a novel host is thought to be a rare outcome following frequent pathogen transfers between host species. However, few opportunities exist to examine whether disease emergence stems from a single successful pathogen transfer, and whether this successful lineage represents only one of several pathogen transfers between hosts. We examined the successful host transfer and subsequent evolution of the bacterial pathogen Mycoplasma gallisepticum, an emergent pathogen of house finches (Haemorhous (formerly Carpodacus) mexicanus). Our principal goals were to assess whether host transfer has been a repeated event between the original poultry hosts and house finches, whether only a single host transfer was ultimately responsible for the emergence of M. gallisepticum in these finches, and whether the spread of the pathogen from east to west across North America has resulted in spatial structuring in the pathogen. Using a phylogeny of M. gallisepticum based on 107 isolates from domestic poultry, house finches and other songbirds, we infer that the bacterium has repeatedly jumped between these two groups of hosts but with only a single lineage of M. gallisepticum persisting and evolving in house finches; bacterial evolution has produced monophyletic eastern and western North American subclades.

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“…This lineage has evolved rapidly, increasing in virulence, likely owing to selection on transmission [18]. In addition to this phenotypic change, exceptionally rapid genomic evolution has been documented in the bacterium [19].…”

Section: Human Impacts On Emerging Infectious Diseases Via Novel Specmentioning

confidence: 99%

Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems

Rogalski

Gowler

Shaw

et al. 2017

Phil. Trans. R. Soc. B

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Humans have contributed to the increased frequency and severity of emerging infectious diseases, which pose a significant threat to wild and domestic species, as well as human health. This review examines major pathways by which humans influence parasitism by altering (co)evolutionary interactions between hosts and parasites on ecological timescales. There is still much to learn about these interactions, but a few well-studied cases show that humans influence disease emergence every step of the way. Human actions significantly increase dispersal of host, parasite and vector species, enabling greater frequency of infection in naive host populations and host switches. Very dense host populations resulting from urbanization and agriculture can drive the evolution of more virulent parasites and, in some cases, more resistant host populations. Human activities that reduce host genetic diversity or impose abiotic stress can impair the ability of hosts to adapt to disease threats. Further, evolutionary responses of hosts and parasites can thwart disease management and biocontrol efforts. Finally, in rare cases, humans influence evolution by eradicating an infectious disease. If we hope to fully understand the factors driving disease emergence and potentially control these epidemics we must consider the widespread influence of humans on host and parasite evolutionary trajectories. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

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Parallel Patterns of Increased Virulence in a Recently Emerged Wildlife Pathogen

Abstract: A bacterial pathogen of wild songbirds evolved higher virulence following its emergence in two separate regions of the host range.

Cited by 86 publications

References 75 publications

Attenuated Phenotype of a Recent House Finch-Associated Mycoplasma gallisepticum Isolate in Domestic Poultry

Attenuated Phenotype of a Recent House Finch-Associated Mycoplasma gallisepticum Isolate in Domestic Poultry

Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen

Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems

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