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Am. J. Trop. Med. Hyg., 75(1), 2006, pp. 70-77
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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POPULATION DYNAMICS OF AN ENDOGENOUS MEIOTIC DRIVE SYSTEM IN AEDES AEGYPTI IN TRINIDAD

SUNG-JAE CHA, DAVE D. CHADEE, AND DAVID W. SEVERSON*
Center for Tropical Disease Research and Training, Department of Biological Sciences University of Notre Dame, Notre Dame, Indiana; Department of Life Sciences, University of the West Indies, St. Augustine, Trinidad, West Indies


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
An endogenous meiotic drive system was previously reported to be segregating in the yellow fever mosquito Aedes aegypti L. (Diptera: Culicidae) population in Trinidad. The meiotic driver (MD) is tightly linked to the male determining locus and selectively targets sensitive responders linked to the female determining allele, causing fragmentation of female gametes. This results in highly male-biased progeny. The MD system was initially studied as a genetic tool for population control with limited success, but recently interest has focused on its potential for population replacement. This study examines the distribution and dynamics of the MD system in Trinidad natural populations. We obtained ovitrap samples from seven geographically distinct regions and determined the allele frequencies of the driver (MD) and sensitive (ms) versus insensitive (mi) responders, respectively. Frequencies of the MD allele ranged from 0.1 to 0.5 and were low at the two major port cities, Port of Spain and San Fernando, suggesting the effects of frequent immigration by non-driving genotypes. Frequencies of the mi allele ranged from 0.4 to 0.7, suggesting the effects of strong selection by the driver. In addition, our results show that the driver and sensitivity of responders in the Trinidad populations are highly polymorphic. Continued studies of the dynamics of the MD system in natural populations are critical to considerations of its use in population replacement.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The remarkable advances in contemporary arthropod genomics offer incredible opportunities to develop and evaluate novel concepts for arthropod-borne disease control, including the genetic manipulation of the arthropod vector to render it incompetent to host and subsequently transmit the pathogen.1 Implicit in efforts to develop strategies to replace highly competent arthropod vector populations with individuals carrying stable anti-pathogen effector genes is the need to identify and develop a genetic system that facilitates a rapid selective sweep of the target transgene. One potential mechanism for promoting population replacement is through agents that cause distortion of Mendelian segregation by meiotic drive.2 In these systems, the meiotic driver product blocks maturation of gametes bearing a sensitive responder locus. The driver gene and responder locus are located on opposite members of homologous chromosomes, respectively. Because driver-carrying chromosomes selectively destroy their homolog, they have the potential for rapidly increasing in frequency in natural populations and theoretically could be engineered to also carry anti-pathogen effector genes, thereby implement population replacement.

Aedes aegypti and Culex pipiens L. mosquito populations have been shown to carry an endogenous meiotic drive system that can distort meiosis in favor of particular gametes.3,4 No sex chromosome dimorphism exists in these species; instead, sex is determined by a single autosomal gene or a small chromosome segment on chromosome 1.5,6 The meiotic drive gene (D) in Ae. aegypti is tightly linked with the male determining allele (M), and the responder locus is tightly linked to the female determining allele (m) on the homologous chromosome.7–9 Alleles at the responder locus can be sensitive (s) or insensitive (i) to the driver gene product. In males heterozygous for the driver and a sensitive responder (MDms), the product of the MD gene acts in trans to cause fragmentation of the ms-bearing gametes during spermatogenesis. Neither the driver gene linked to a female determining allele (mD) nor the responder linked to the male determining allele (Ms) functions properly to produce the drive phenotype.10 Although the molecular basis for the MD system is unknown, the observed phenotype in Ae. aegypti is a highly male-biased sex ratio.

Previous studies of the MD system in Ae. aegypti focused on investigating its potential as a novel mosquito control strategy.8,11–13 Based on the concept that the release of a strong meiotic driver into drive sensitive populations should result in increasingly male-biased populations, it was hypothesized that these populations could be driven to extinction. Curtis and others12 combined the meiotic drive system with double translocation heterozygotes (T1T3) to test for Ae. aegypti population suppression in field cage experiments, and successfully achieved population eradication. Hickey and Craig8 performed cage experiments designed to test the effect of the meiotic driver for genetic control of Ae. aegypti. Cage populations were manipulated to introduce strong driver males into sensitive female cage populations. Although male-biased sex ratios were observed for 10 generations, sex ratio distortion declined beginning at the F3 generation and eventually reverted to a 1:1 ratio by the F11 generation. However, when they duplicated these experiments with a stronger drive strain and the same sensitive strain, they obtained population extinction after 43 weeks. To explain the reversion of sex ratio distortion in the former experiment, Hickey and Craig suggested the accumulation of drive suppressors in the female population,7,8 and this was later supported by the identification of a tolerance gene in the RED strain by Wood and Ouda.14 In addition to suppressors, driver insensitive responders exist in natural populations under non-driving conditions.15 Therefore, selection for a drive suppressor or insensitive responder would inhibit population suppression by the meiotic driver. However, Wood and others13 showed that the meiotic driver has strong population replacement potential. They introduced males containing the red-eye marker gene linked to a strong driver allele into sensitive black eyed mosquito populations. Although the red-eye marker alleles showed some unexpected tendencies for increasing, the MD alleles showed strong allele replacement potential. By the F15 generation, the driver population consisted of 62% red-eyed mosquitoes. Recently, cage studies have shown that the MD system can effect significant targeted allele replacement when introduced into sensitive populations.16

In conjunction with efforts to determine the feasibility of meiotic drive as a population replacement strategy, it is important to understand the population dynamics of the drive system in natural Ae. aegypti populations. Hickey and Craig7 reported varying degrees of the strength of the meiotic driver and sensitivity of its responder in the Ae. aegypti population in Trinidad. In addition, Wood17 categorized responder sensitivities in the T30 strain, derived from the Trinidad field population, into six groups based on the sex ratios. In previous studies, genetic polymorphism in the MD system was apparent in a laboratory strain (WART).7 Therefore, the dynamics of the MD system in Ae. aegypti populations will be determined largely by the strength of the driver alleles, variability in sensitivity of the responder alleles, and their relative frequencies.

The existence of a strong meiotic driver within the Ae. aegypti Trinidad population has repeatedly been confirmed since the 1950s.7,8,12,17–20 Trinidad is, therefore, one of the most ideal places to study the population dynamics of the Ae. aegypti meiotic drive system. The Ae. aegypti populations throughout the Caribbean experienced a significant genetic bottleneck in the early 1960s because of an intensive vector control program, largely through the widespread usage of DDT under the direction of the Pan American Health Organization (PAHO). By 1962, 18 continental countries and several Caribbean island countries had successfully achieved eradication.21 Although the program officially ended in 1970 in the United States, after 1962, the number of Ae. aegypti–free countries declined quickly as rapid re-infestation by Ae. aegypti was reported.22 However, after the end of the PAHO program, the Ae. aegypti eradication program in Trinidad and Tobago continued from 1976 to 1981 under the direction of the Ministry of Health.23 Interestingly, presence of the meiotic driver was reported before and after the population bottleneck and still exists at a relatively high frequency in Trinidad natural populations.8,18,19 To study the distribution and dynamics of the meiotic drive system in Trinidad, we selected seven locations and set up ovitraps for sampling Ae. aegypti populations. To determine drive genotypes, we followed the general mating scheme outlined by Hickey and Craig.7 In our test crosses, observed sex ratios indicated the individual genotypes and an estimation of the driver strength or the responder sensitivities. Allele frequencies of the driver and responder were determined and compared among all seven Trinidad locations.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Collection of samples. Seven geographically distinct locations in Trinidad were selected for sampling Ae. aegypti (Figure 1Go). During February to April 2004, 10–20 ovitraps24 were distributed at each location. Two ovitraps were set at each house: one inside and the other outside. Ovitraps consisted of a black plastic cup (400-mL volume) with {approx}250 mL of water, into which a 12.5 x 2.5-cm hardboard paddle was placed in an upright manner. Female Ae. aegypti mosquitoes will readily oviposit on the paddle near the water interface.25 After 7 days, the paddles were collected and dried for transport to the laboratory at the University of Notre Dame. Ovitraps were maintained for a period sufficient to ensure that eggs were obtained from at least 10 paddles per location.


Figure 1
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  		    FIGURE 1. Map of Trinidad showing locations selected for sampling Ae. aegypti populations.

 
Rearing and genetic crosses. Each egg paddle was placed into a separate container for hatching and rearing into adults. Ten paddles per study site were selected and hatched. Rearing was conducted in an environmental chamber held at 26°C, 84% relative humidity, and a 16-hour light/8-hour dark cycle with a 1-hour crepuscular period at the beginning and end of each cycle. Larvae were reared on a bovine liver powder suspension, and adults were supplied with cotton balls soaked in 5% sugar solution. Female mosquitoes were blood fed on anesthetized rats. Our protocol for maintenance and care of experimental animals was reviewed and approved by the Institutional Animal Care and Use Committee at the University of Notre Dame. Animals are maintained and cared for in the Freimann Life Science Center, an AAALAC accredited facility.

Crosses to identify genotypes at the meiotic driver locus and its responder were prepared generally following the mating scheme outlined by Hickey and Craig.7 Genetic stocks for this experiment were the Ae. aegypti T37 and RED strains. The T37 strain carries a strong meiotic driver and insensitive responder.19 T37 strain males (genotype MDmi) were used to test field-collected females for their responder genotype. The RED strain carries a highly sensitive responder.8,19 RED strain females (genotype msms) were used to test field-collected males for their driver genotype. With progeny from each egg paddle, two test crosses were set up: 1) a field male and five RED strain females and 2) a T37 strain male and five field females. Each test cross was replicated five times to ensure successful mating and oviposition by at least one pair for the male and female test crosses, respectively, for each paddle. From these, one F1 family was randomly selected to prepare seven BC1 families by pairwise mating of one male and three RED females. After mating and blood feeding, females from all crosses were transferred individually to small glass vials containing {approx} 1 mL H2O and a paper towel strip for oviposition. After oviposition, the egg papers were dried and stored at 16°C until hatched.

Sex ratio and genotyping. Sex ratios observed among progeny from the male test and female test crosses were used to assess genotypes at the driver locus as outlined in Figure 2Go. Departures from the expected male to female ratio were determined using the {chi}2 test.26 Because Ae. aegypti crosses generally reflect a slight bias for male progeny under non-driving conditions and could show significance at the P = 0.05 level if tested for an expected 1:1 sex ratio,8 we elected to test for an expected 0.535:0.465 male to female ratio based on the previously observed sex ratios among progeny from matings within the RED strain.19 For each field-collected male, sex ratios were determined for five F1 and six BC1 families. A male-biased sex ratio in the F1 indicated that the male was MDms genotype. A normal sex ratio in the F1 and male biased sex ratio in the BC1 indicated that the male was MDmi genotype. No sex ratio distortion in the F1 or BC1 indicated the male carried a non-driving allele (Md). The number of males and females from the five F1 families were summed to determine the sex ratio. If less than four of six BC1 families showed a significant departure from a 1:1 sex ratio, the male was classified as a non-driver. Field-collected females were genotyped at the responder locus by examining sex ratios in the BC1 generation. Females with the mimi genotype reflect 1:1 sex ratios in the BC1 generation. Females with the msms genotype have male biased BC1 families, whereas females with the msmi genotype have a mixture of male biased and normal sex ratio BC1 families.


Figure 2
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  		    FIGURE 2. Test cross strategy for identifying males carrying the meiotic driver and sensitivity to drive of females. MD = driver allele; Md = non-driver allele; Ms = sensitive responder allele; mi = insensitive responder allele. Modified after Hickey and Craig.7

 
Genotype data were converted into allele frequencies at the driver and responder loci for each of the seven sample locations. The mean sex ratios of the six BC1 families were determined to show the strength of the drive alleles for each male test and the responder sensitivities for the female test, respectively. For heterozygous females, the mean sex ratio was determined from male-biased BC1 families for the sensitive responder and the mean sex ratio from the 1:1 families for the insensitive responder, respectively.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Sex ratio and genotyping. Sex ratios and inferred genotypes at the meiotic driver locus, based on testing males reared from eggs collected at seven locations in Trinidad, are shown in Table 1Go. Genotypes were determined based on the assumption that male-biased sex ratios were caused by the meiotic drive gene products affecting random segregation of the gametes. Frequencies of the MD allele ranged from 0.1 to 0.5 (Table 2Go), with the highest frequency observed in samples collected at Curepe. The mean allele frequencies of the meiotic driver and non-driver were 0.26 ± 0.14 and 0.74 ± 0.14, respectively.


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TABLE 1
Observed sex ratios and inferred genotypes at the drive gene locus in male test crosses
 

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TABLE 2
Observed allele frequencies of the meiotic drive system at each sample location in Trinidad
 
Sex ratios and inferred genotypes at the responder locus are shown in Table 3Go. Frequencies of the ms allele ranged from 0.3 to 0.6 (Table 2Go). The highest frequency was observed in samples collected at Fyzabad. Frequencies of the mi allele ranged from 0.40 to 0.70. The highest frequency was observed in samples from Valencia. Heterozygous females were predominant at all the locations. The mean allele frequencies of the sensitive responder and insensitive responder were 0.42 ± 0.10 and 0.58 ± 0.10, respectively.


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TABLE 3
Observed sex ratios and inferred genotypes at the responder locus in female test crosses
 
Observed frequencies of the MD allele did not show significant correlation with observed frequencies of the mi allele (r = 0.17), suggesting that the two loci are not at equilibrium within sites and, therefore, likely reflect the results of continual migration within the island and immigration from outside sources caused largely by human activities.

Sex ratio distortion. The observed variations in sex ratio distortion by driver alleles carried by field-derived males are shown in Figure 3AGo. The frequency of a strong driver allele (< 12.5% female) was < 3% across the island. The mean BC1 sex ratio associated with the MD alleles was 25.5% female. The observed sex ratio distribution from testing field-derived females is shown in Figure 3BGo. Previously, Wood17 classified responder loci into six groups according to their sensitivities to the driver. Although our data do not fit this discrete classification very well, the observed frequency distribution of sex ratios is similar to results observed with the T30 strain. The frequency of a highly sensitive responder (< 12.5% female) was < 2.5% across the island. The mean BC1 sex ratio associated with the ms allele was 29.1% female.


Figure 3
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  		    FIGURE 3. Distribution of percentage of females among the BC, progeny of single F1 males derived from two test crosses. A, Trinidad males x RED females (mimi), where sex ratios indicate the drive strength. B, T37 (MDmi) males x Trinidad females, where sex ratios indicate the responder sensitivities. Samples from all locations were combined. Mean sex ratios were determined and are shown for each allele.

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The best-characterized meiotic drive system is the segregation distorter (SD) in Drosophila melanogaster.27 With D. melanogaster, SD is found at frequencies of 1–5% in most natural populations.28–31 Temin and Marthas examined the population dynamics of SD for 3 years in Madison, WI, and Sonoma County, CA,30 and compared their data with a study conducted 25 years previously.31 Their estimates for SD frequency across 3 years were consistently less than that observed in the earlier study 3%, indicating that a selective sweep of the SD gene through these populations had not occurred. Two hypotheses have been proposed to explain this phenomena including: 1) that populations challenged by SD also contain suppressors or insensitive responders in high frequencies, which prevent SD sweeps,32–35 and 2) that the insensitive responders have significant fitness costs under non-driving conditions and that the low frequency of SD is caused by its short evolutionary history.36,37 Although population frequencies of the insensitive responder (Rspi) are highly polymorphic, ranging from 3% to 86%, with mean values of 45%, Rspi frequencies are usually higher than the SD allele frequency in natural populations,32,34,38–40 thus providing support for the first hypothesis.

Our studies of Ae. aegypti populations in Trinidad show similarity to that observed in D. melanogaster populations as the frequencies of insensitive responders were consistently higher than the frequencies of driver alleles. In addition, Suguna and Wood41 reported the presence of insensitive responders after testing strong drive strains against drive-free natural populations in India. It also is evident that the degree of distortion observed in Trinidad field populations is lower than in test crosses using the sensitive RED strain. That is, the mean F1 sex ratio of field-collected driving males carrying a sensitive responder (MDms) was 37.34 ± 3.23% female, whereas their BC1 mean sex ratio that reflects the RED strain responder sensitivity was 21.34 ± 12.08 female. This corresponds well with our previous studies.19

It has been suggested that the polymorphism observed in driver strength and responder sensitivities in natural populations is caused by balancing selection. Wood17 reported between-family variation in sex ratios within the Trinidad-derived Ae. aegypti T30 strain and suggested that there were at least six different alleles with varying sensitivity at the responder locus. Our data also reflect considerable polymorphism in sex ratio between sib-families. For example, the Curepe no. 5 male in Table 1Go showed highly polymorphic sex ratios ranging from 7.46% to 42.51% female in the BC1 generation. In some cases, a number of our BC1 families showed a mixture of distorted and 1:1 sex ratios, indicating the loss of or suppression of driver effects. Because the observed within-male sex ratio polymorphisms were derived from single responder and driver alleles, our data suggest that there are other factors influencing the observed sex ratios, in addition to the responder sensitivities or driver strength in the Trinidad population. Wood and Ouda14 also reported the existence of two driver suppressors and one enhancer within A. aegypti laboratory strains. Another factor maintaining balanced polymorphism in the Trinidad population could be recombination. Recombination between the male determining locus (M) and driver gene (D) would result in the loss of the drive allele in male-determining gametes. Indeed, a recombination frequency of 1.2% between M and D was reported for one of the strong meiotic driver strains (ACCRA).17

Our data show that both the strength of drivers and the sensitivity of responders in the Trinidad field populations are highly polymorphic (Figure 3Go). The distribution of the responder sensitivities in Trinidad populations (Figure 3BGo) is in contrast with previous data for an Ae. aegypti population in India, in which no driver allele was found.41 The frequency of a highly sensitive responder (< 12.5% female) was much lower in the Trinidad population than the Indian population, which implies that the driver males are selecting against the sensitive responders. Our data confirmed previous studies of the meiotic drive system in the Trinidad Ae. aegypti population, which indicated relatively high frequencies of driver males19 and varying degrees of responder sensitivities.7,19 The mean frequency of driving males and insensitive responders was 0.26 and 0.58, respectively. The highest driver frequency was observed in the Curepe population. Similar, although slightly lower (0.43) frequencies in the Curepe population were reported previously.17 Furthermore, our previous cage trials designed to test the impact of releasing males carrying a strong driver and insensitive responder into populations carrying sensitive responders showed strong selection for insensitive responder alleles.16

There was no obvious pattern to the observed distribution in the MD system among all seven sampling locations. However, given the relatively small sample sizes at each location, our statistical power to evaluate differences among locations is limited. Furthermore, other studies have verified that considerable gene flow occurs among Ae. aegypti populations between Caribbean islands and the mainland and within Trinidad.42–44 This implies that continuous migration through human activities likely impacts the population dynamics of the MD system in Trinidad. However, while population genotypes at neutral marker loci were not determined for this study, we noted that an earlier study showed small, but significant, pairwise FST estimates for three locations in Trinidad; these included two locations from this study (Curepe and San Fernando), indicating that some population substructure exists within Trinidad populations, and therefore the observed inter-population differences in MD frequency may be valid.43 Interestingly, driver allele frequencies at the two major shipping port areas (Port of Spain and San Fernando) were among the lowest we observed, suggesting the likelihood that non-driving alleles may frequently be imported. In addition, repeated pesticide applications that result in periodic population bottlenecks may also be affecting the dynamics of the MD system in Trinidad.43

Finally, the distribution of the MD system among Ae. aegypti populations is not worldwide, and in some regions, the MD allele has been reported as completely absent.9,19 The high MD allele frequencies that have consistently been observed in Trinidad have not been observed elsewhere. For example, previous examinations of five strains/populations including Trinidad indicated that, whereas four of the five carried the MD allele, the frequency was low (0.13 maximum) in all but the Trinidad population (0.43).19 The mean frequency across Trinidad in this study was lower (0.26), but still high compared with populations in the earlier study. Therefore, the meiotic drive approach does have potential for development as a novel population replacement strategy in drive sensitive populations. This is dependent on continued studies of the population dynamics of the drive system and its complete molecular characterization.

Received October 27, 2005. Accepted for publication March 13, 2006.

Financial support: This work was supported by NIH NIAID Grant PO1-AI45123.

* Address correspondence to David W. Severson, Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556. E-mail: severson.1{at}nd.edu Back

Authors’ addresses: Sung-Jae Cha, Johns Hopkins School of Public Health, Malaria Research Institute, Department of Molecular Microbiology and Immunology, 615 North Wolfe Street, Baltimore, MD 21205, E-mail: scha{at}jhsph.edu. Dave D. Chadee, Department of Life Sciences, University of the West Indies, St. Augustine, Trinidad, West Indies, E-mail: chadee{at}tstt.net.tt. David W. Severson, Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556.

Reprint requests: David W. Severson, Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, E-mail: severson.1{at}nd.edu.


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 DISCUSSION
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