Cargando…

Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics

Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. H...

Descripción completa

Detalles Bibliográficos
Autores principales: Rudicell, Rebecca S., Holland Jones, James, Wroblewski, Emily E., Learn, Gerald H., Li, Yingying, Robertson, Joel D., Greengrass, Elizabeth, Grossmann, Falk, Kamenya, Shadrack, Pintea, Lilian, Mjungu, Deus C., Lonsdorf, Elizabeth V., Mosser, Anna, Lehman, Clarence, Collins, D. Anthony, Keele, Brandon F., Goodall, Jane, Hahn, Beatrice H., Pusey, Anne E., Wilson, Michael L.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2944804/
https://www.ncbi.nlm.nih.gov/pubmed/20886099
http://dx.doi.org/10.1371/journal.ppat.1001116
_version_ 1782187131288944640
author Rudicell, Rebecca S.
Holland Jones, James
Wroblewski, Emily E.
Learn, Gerald H.
Li, Yingying
Robertson, Joel D.
Greengrass, Elizabeth
Grossmann, Falk
Kamenya, Shadrack
Pintea, Lilian
Mjungu, Deus C.
Lonsdorf, Elizabeth V.
Mosser, Anna
Lehman, Clarence
Collins, D. Anthony
Keele, Brandon F.
Goodall, Jane
Hahn, Beatrice H.
Pusey, Anne E.
Wilson, Michael L.
author_facet Rudicell, Rebecca S.
Holland Jones, James
Wroblewski, Emily E.
Learn, Gerald H.
Li, Yingying
Robertson, Joel D.
Greengrass, Elizabeth
Grossmann, Falk
Kamenya, Shadrack
Pintea, Lilian
Mjungu, Deus C.
Lonsdorf, Elizabeth V.
Mosser, Anna
Lehman, Clarence
Collins, D. Anthony
Keele, Brandon F.
Goodall, Jane
Hahn, Beatrice H.
Pusey, Anne E.
Wilson, Michael L.
author_sort Rudicell, Rebecca S.
collection PubMed
description Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002–2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of −6.5% to −7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002–2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen.
format Text
id pubmed-2944804
institution National Center for Biotechnology Information
language English
publishDate 2010
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-29448042010-09-30 Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics Rudicell, Rebecca S. Holland Jones, James Wroblewski, Emily E. Learn, Gerald H. Li, Yingying Robertson, Joel D. Greengrass, Elizabeth Grossmann, Falk Kamenya, Shadrack Pintea, Lilian Mjungu, Deus C. Lonsdorf, Elizabeth V. Mosser, Anna Lehman, Clarence Collins, D. Anthony Keele, Brandon F. Goodall, Jane Hahn, Beatrice H. Pusey, Anne E. Wilson, Michael L. PLoS Pathog Research Article Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002–2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of −6.5% to −7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002–2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen. Public Library of Science 2010-09-23 /pmc/articles/PMC2944804/ /pubmed/20886099 http://dx.doi.org/10.1371/journal.ppat.1001116 Text en This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Rudicell, Rebecca S.
Holland Jones, James
Wroblewski, Emily E.
Learn, Gerald H.
Li, Yingying
Robertson, Joel D.
Greengrass, Elizabeth
Grossmann, Falk
Kamenya, Shadrack
Pintea, Lilian
Mjungu, Deus C.
Lonsdorf, Elizabeth V.
Mosser, Anna
Lehman, Clarence
Collins, D. Anthony
Keele, Brandon F.
Goodall, Jane
Hahn, Beatrice H.
Pusey, Anne E.
Wilson, Michael L.
Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title_full Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title_fullStr Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title_full_unstemmed Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title_short Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics
title_sort impact of simian immunodeficiency virus infection on chimpanzee population dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2944804/
https://www.ncbi.nlm.nih.gov/pubmed/20886099
http://dx.doi.org/10.1371/journal.ppat.1001116
work_keys_str_mv AT rudicellrebeccas impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT hollandjonesjames impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT wroblewskiemilye impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT learngeraldh impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT liyingying impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT robertsonjoeld impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT greengrasselizabeth impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT grossmannfalk impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT kamenyashadrack impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT pintealilian impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT mjungudeusc impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT lonsdorfelizabethv impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT mosseranna impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT lehmanclarence impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT collinsdanthony impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT keelebrandonf impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT goodalljane impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT hahnbeatriceh impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT puseyannee impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics
AT wilsonmichaell impactofsimianimmunodeficiencyvirusinfectiononchimpanzeepopulationdynamics