#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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. 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.


Vyšlo v časopise: Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001116
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001116

Souhrn

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.


Zdroje

1. SilvestriG

2008 Immunity in natural SIV infections. J Intern Med 265 97 109

2. KeeleBF

JonesJH

TerioKA

EstesJD

RudicellRS

2009 Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460 515 519

3. WalshPD

AbernethyKA

BermejoM

BeyersR

De WachterP

2003 Catastrophic ape decline in western equatorial Africa. Nature 422 611 614

4. CampbellG

KuehlH

N'Goran KouaméP

BoeschC

2008 Alarming decline of West African chimpanzees in Côte d'Ivoire. Curr Biol 18 R903 R904

5. KöndgenS

KühlH

N'GoranPK

WalshPD

SchenkSS

2008 Pandemic human viruses cause decline of endangered great apes. Curr Biol 18 1 5

6. HahnBH

ShawGM

De CockKM

SharpPM

2000 AIDS as a zoonosis: scientific and public health implications. Science 287 607 614

7. AghokengAF

AyoubaA

Mpoudi NgoleE

LoulS

LiegeoisF

2010 Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infect Genet Evol 10 386 396

8. Phillips-ConroyJE

JollyCJ

PetrosB

AllanJS

DesrosiersRC

1994 Sexual transmission of SIVagm in wild grivet monkeys. J Med Primatol 23 1 7

9. SantiagoML

RangeF

KeeleBF

LiYY

BailesE

2005 Simian immunodeficiency virus infection in free-ranging sooty Mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: Implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79 12515 12527

10. SantiagoML

LukasikM

KamenyaS

LiY

Bibollet-RucheF

2003 Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J Virol 77 7545 7562

11. KeeleBF

Van HeuverswynF

LiY

BailesE

TakehisaJ

2006 Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313 523 526

12. LiY

NdjangoJ-B

LearnGH

RobertsonJ

TakehisaJ

2010 Molecular epidemiology of simian immunodeficiency virus in eastern chimpanzees and gorillas. 17th Conference on Retroviruses and Opportunistic Infections; 16–19 February 2010; San Francisco, California. CROI 2010. [Abstract 440]

13. WorobeyM

SantiagoML

KeeleBF

NdjangoJBN

JoyJB

2004 Origin of AIDS - Contaminated polio vaccine theory refuted. Nature 428 820 820

14. SharpPM

ShawGM

HahnBH

2005 Simian immunodeficiency virus infection of chimpanzees. J Virol 79 3891 3902

15. PuseyAE

PinteaLP

WilsonML

KamenyaS

GoodallJ

2007 The contribution of long-term research at Gombe National Park to chimpanzee conservation. Conserv Biol 21 623 634

16. GreengrassE

2000 The sudden decline of a community of chimpanzees at Gombe National Park. Pan Africa News 7

17. GoodallJ

1986 The Chimpanzees of Gombe: Patterns of Behavior Cambridge, Massachusetts Belknap Press. 673

18. PuseyAE

WilsonML

CollinsDA

2008 Human impacts, disease risk, and population dynamics in the chimpanzees of Gombe National Park, Tanzania. Am J Primatol 70 738 744

19. SantiagoML

RodenburgCM

KamenyaS

Bibollet-RucheF

GaoF

2002 SIVcpz in wild chimpanzees. Science 295 465

20. PuseyAE

1979 Intercommunity transfer of chimpanzees in Gombe National Park

HamburgDA

McCownER

The Great Apes Menlo Park Benjamin/Cummings 464 479

21. HuschB

BeersTW

KershawJA

2003 Forest Mensuration Hoboken John Wiley & Sons, Inc. 456

22. LacyRC

1993 Vortex - a computer-simulation model for population viability analysis. Wildl Res 20 45 65

23. GrayRH

WawerMJ

BrookmeyerR

SewankamboNK

SerwaddaD

2001 Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357 1149 1153

24. WranghamRW

WilsonML

MullerMN

2006 Comparative rates of violence in chimpanzees and humans. Primates 47 14 26

25. MitaniJC

WattsDP

MullerMN

2002 Recent developments in the study of wild chimpanzee behavior. Evol Anthropol 11 9 25

26. NishidaT

KawanakaK

1985 Within-group cannibalism by adult male chimpanzees. Primates 26 274 284

27. WilsonML

WranghamRW

2003 Intergroup relations in chimpanzees. Annu Rev Anthropol 32 363 392

28. NishidaT

Hiraiwa-HasegawaM

HasegawaT

TakahataY

1985 Group extinction and female transfer in wild chimpanzees in the Mahale National Park, Tanzania. Z Tierpsychol 67 284 301

29. van der PaalL

ShaferLA

ToddJ

MayanjaBN

WhitworthJAG

2007 HIV-1 disease progression and mortality before the introduction of highly active antiretroviral therapy in rural Uganda. AIDS 21 S21 S29

30. HladikF

McElrathMJ

2008 Setting the stage: host invasion by HIV. Nat Rev 8 447 457

31. MorinPA

ChambersKE

BoeschC

VigilantL

2001 Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10 1835 1844

32. ConstableJL

AshleyMV

GoodallJ

PuseyAE

2001 Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10 1279 1300

33. WroblewskiEE

MurrayCM

KeeleBF

Schumacher-StankeyJ

HahnBH

2009 Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77 873 885

34. MarshallTC

SlateJ

KruukLEB

PembertonJM

1998 Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7 639 655

35. GoodnightKF

QuellerDC

1999 Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8 1231 1234

36. QuellerDC

GoodnightKF

1989 Estimating relatedness using genetic-markers. Evolution 43 258 275

37. LarkinMA

BlackshieldsG

BrownNP

ChennaR

McGettiganPA

2007 Clustal W and clustal X version 2.0. Bioinformatics 23 2947 2948

38. RonquistF

HuelsenbeckJP

2003 MrBayes 3:Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574

39. PlumptreAJ

ReynoldsV

1996 Censusing chimpanzees in the Budongo forest, Uganda. Int J Primatol 17 85 99

40. ThomasL

BucklandST

RexstadEA

LaakeJL

StrindbergS

2010 Distance software: design and analysis of distance sampling surveys for estimating population size. J Appl Ecol 47 5 14

41. PlumptreAJ

ReynoldsV

1997 Nesting behavior of chimpanzees: Implications for censuses. Intern J Primatol 18 475 485

42. PlumptreAJ

2000 Monitoring mammal populations with line transect techniques in African forests. J Appl Ecol 37 356 368

43. WilsonML

WallauerW

PuseyAE

2004 New cases of intergroup violence among chimpanzees in Gombe National Park, Tanzania. Int J Primatol 25 523 549

44. MurrayCM

EberlyLE

PuseyAE

2006 Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behav Ecol 17 1020 1028

45. PinteaL

2007 Applying satellite imagery and GIS for chimpanzee habitat change detection and conservation [PhD Thesis] St. Paul University of Minnesota

46. SchafferWM

1974 Optimal reproductive effort in fluctuating environments. Am Nat 108 783 790

47. GillespieDT

1977 Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81 2340 2361

48. DiekmannO

HeesterbeekH

2000 Mathematical epidemiology of infectious diseases: Model building, analysis and interpretation Chichester UK John Wiley & Son, LTD. 303

49. AndersonRM

MayRM

1991 Infectious Diseases of Humans: Dynamics and Control Oxford, UK Oxford University Press. 768

50. MorrisM

1991 A log-linear modeling framework for selective mixing. Math Biosci 107 349 377

51. PuseyAE

1990 Behavioural changes at adolescence in chimpanzees. Behaviour 115 203 246

52. Emery ThompsonM

2005 Reproductive endocrinology of wild chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am J Primatol 67 137 158

53. HillK

BoeschC

GoodallJ

PuseyAE

WilliamsJM

WranghamRW

2001 Mortality rates among wild chimpanzees. J Hum Evol 40 437 450

54. CaswellH

2001 Matrix Population Models: Construction, Analysis and Interpretation Sunderland, MA Sinauer Associates, Inc. 722

55. Van HeuverswynF

LiY

BailesE

NeelC

LafayB

2007 Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 368 155 171

56. KeelingMJ

RohaniP

2007 Modeling Infectious Diseases in Humans and Animals Princeton, NJ Princeton University Press. 408

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2010 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#