Gametocyte sex ratios as indirect measures of outcrossing rates in malaria

Andrew Fraser Read, A. E. Keymer, A. Narara, S. Nee, K. P. Day

Research output: Contribution to journalArticle

94 Citations (Scopus)

Abstract

The frequency of recombination between unlike genotypes is central to understanding the generation of genetic diversity in natural populations of malaria. Here we suggest a way of investigating the problem which could complement conventional biochemical approaches to the population genetics of malaria. Sex allocation theory is one of the most successful areas of evolutionary biology. A well-supported prediction is that progressively less female-biased sex ratios are favoured with more outcrossing; equal numbers of males and females being evolutionarily stable in randomly mating outbred populations. We present a simple game theory model to support the idea that outcrossing rates in malaria will be correlated with the sex ratio of gametocytes in the peripheral blood of vertebrate hosts. Blood films from epidemiological surveys and culture-adapted isolates from Madang Province, Papua New Guinea, were used to estimate average gametocyte sex ratio of Plasmodium falciparum in the area. The geometric mean proportion of males in the population was 0.18 (95% confidence limits: 0.15-0.22). From our model, we estimate that, on average, 36 % of zygotes are the result of outcrossing. This estimate assumes that most microgametes released following exflagellation are capable of fertilization. If, on average, fewer than about 70 % of microgametes are capable of fertilization (as is the case in at least one other species of Plasmodium), the observed sex ratio would be consistent with between zero and 36%, of zygotes being the result of outcrossing. These estimates suggest that there is usually a numerically dominant genotype in the gametocyte population in a blood meal, and that a considerable amount of selfing is occurring in P. falciparum populations in the Madang region, even though it is an area of intense year-round transmission.

Original languageEnglish (US)
Pages (from-to)387-395
Number of pages9
JournalParasitology
Volume104
Issue number3
DOIs
StatePublished - Jan 1 1992

Fingerprint

gametocytes
Sex Ratio
outcrossing
malaria
Malaria
sex ratio
Population
Zygote
Plasmodium falciparum
zygote
fertilization (reproduction)
Fertilization
Genotype
Game Theory
Papua New Guinea
game theory
sex allocation
Plasmodium
genotype
blood

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Animal Science and Zoology
  • Infectious Diseases

Cite this

Read, Andrew Fraser ; Keymer, A. E. ; Narara, A. ; Nee, S. ; Day, K. P. / Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. In: Parasitology. 1992 ; Vol. 104, No. 3. pp. 387-395.
@article{a01af867e79b41ed9202694b7ac69e49,
title = "Gametocyte sex ratios as indirect measures of outcrossing rates in malaria",
abstract = "The frequency of recombination between unlike genotypes is central to understanding the generation of genetic diversity in natural populations of malaria. Here we suggest a way of investigating the problem which could complement conventional biochemical approaches to the population genetics of malaria. Sex allocation theory is one of the most successful areas of evolutionary biology. A well-supported prediction is that progressively less female-biased sex ratios are favoured with more outcrossing; equal numbers of males and females being evolutionarily stable in randomly mating outbred populations. We present a simple game theory model to support the idea that outcrossing rates in malaria will be correlated with the sex ratio of gametocytes in the peripheral blood of vertebrate hosts. Blood films from epidemiological surveys and culture-adapted isolates from Madang Province, Papua New Guinea, were used to estimate average gametocyte sex ratio of Plasmodium falciparum in the area. The geometric mean proportion of males in the population was 0.18 (95{\%} confidence limits: 0.15-0.22). From our model, we estimate that, on average, 36 {\%} of zygotes are the result of outcrossing. This estimate assumes that most microgametes released following exflagellation are capable of fertilization. If, on average, fewer than about 70 {\%} of microgametes are capable of fertilization (as is the case in at least one other species of Plasmodium), the observed sex ratio would be consistent with between zero and 36{\%}, of zygotes being the result of outcrossing. These estimates suggest that there is usually a numerically dominant genotype in the gametocyte population in a blood meal, and that a considerable amount of selfing is occurring in P. falciparum populations in the Madang region, even though it is an area of intense year-round transmission.",
author = "Read, {Andrew Fraser} and Keymer, {A. E.} and A. Narara and S. Nee and Day, {K. P.}",
year = "1992",
month = "1",
day = "1",
doi = "10.1017/S0031182000063630",
language = "English (US)",
volume = "104",
pages = "387--395",
journal = "Parasitology",
issn = "0031-1820",
publisher = "Cambridge University Press",
number = "3",

}

Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. / Read, Andrew Fraser; Keymer, A. E.; Narara, A.; Nee, S.; Day, K. P.

In: Parasitology, Vol. 104, No. 3, 01.01.1992, p. 387-395.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Gametocyte sex ratios as indirect measures of outcrossing rates in malaria

AU - Read, Andrew Fraser

AU - Keymer, A. E.

AU - Narara, A.

AU - Nee, S.

AU - Day, K. P.

PY - 1992/1/1

Y1 - 1992/1/1

N2 - The frequency of recombination between unlike genotypes is central to understanding the generation of genetic diversity in natural populations of malaria. Here we suggest a way of investigating the problem which could complement conventional biochemical approaches to the population genetics of malaria. Sex allocation theory is one of the most successful areas of evolutionary biology. A well-supported prediction is that progressively less female-biased sex ratios are favoured with more outcrossing; equal numbers of males and females being evolutionarily stable in randomly mating outbred populations. We present a simple game theory model to support the idea that outcrossing rates in malaria will be correlated with the sex ratio of gametocytes in the peripheral blood of vertebrate hosts. Blood films from epidemiological surveys and culture-adapted isolates from Madang Province, Papua New Guinea, were used to estimate average gametocyte sex ratio of Plasmodium falciparum in the area. The geometric mean proportion of males in the population was 0.18 (95% confidence limits: 0.15-0.22). From our model, we estimate that, on average, 36 % of zygotes are the result of outcrossing. This estimate assumes that most microgametes released following exflagellation are capable of fertilization. If, on average, fewer than about 70 % of microgametes are capable of fertilization (as is the case in at least one other species of Plasmodium), the observed sex ratio would be consistent with between zero and 36%, of zygotes being the result of outcrossing. These estimates suggest that there is usually a numerically dominant genotype in the gametocyte population in a blood meal, and that a considerable amount of selfing is occurring in P. falciparum populations in the Madang region, even though it is an area of intense year-round transmission.

AB - The frequency of recombination between unlike genotypes is central to understanding the generation of genetic diversity in natural populations of malaria. Here we suggest a way of investigating the problem which could complement conventional biochemical approaches to the population genetics of malaria. Sex allocation theory is one of the most successful areas of evolutionary biology. A well-supported prediction is that progressively less female-biased sex ratios are favoured with more outcrossing; equal numbers of males and females being evolutionarily stable in randomly mating outbred populations. We present a simple game theory model to support the idea that outcrossing rates in malaria will be correlated with the sex ratio of gametocytes in the peripheral blood of vertebrate hosts. Blood films from epidemiological surveys and culture-adapted isolates from Madang Province, Papua New Guinea, were used to estimate average gametocyte sex ratio of Plasmodium falciparum in the area. The geometric mean proportion of males in the population was 0.18 (95% confidence limits: 0.15-0.22). From our model, we estimate that, on average, 36 % of zygotes are the result of outcrossing. This estimate assumes that most microgametes released following exflagellation are capable of fertilization. If, on average, fewer than about 70 % of microgametes are capable of fertilization (as is the case in at least one other species of Plasmodium), the observed sex ratio would be consistent with between zero and 36%, of zygotes being the result of outcrossing. These estimates suggest that there is usually a numerically dominant genotype in the gametocyte population in a blood meal, and that a considerable amount of selfing is occurring in P. falciparum populations in the Madang region, even though it is an area of intense year-round transmission.

UR - http://www.scopus.com/inward/record.url?scp=0026704442&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0026704442&partnerID=8YFLogxK

U2 - 10.1017/S0031182000063630

DO - 10.1017/S0031182000063630

M3 - Article

C2 - 1641238

AN - SCOPUS:0026704442

VL - 104

SP - 387

EP - 395

JO - Parasitology

JF - Parasitology

SN - 0031-1820

IS - 3

ER -