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Sex-dependent infection causes nonadditive effects on kissing bug fecundity.

ABSTRACT: The influence of parasites on host reproduction has been widely studied in natural and experimental conditions. Most studies, however, have evaluated the parasite impact on female hosts only, neglecting the contribution of males for host reproduction. This omission is unfortunate as sex-dependent infection may have important implications for host-parasite associations. Here, we evaluate for the first time the independent and nonindependent effects of gender infection on host reproductive success using the kissing bug Mepraia spinolai and the protozoan Trypanosoma cruzi as model system. We set up four crossing treatments including the following: (1) both genders infected, (2) both genders uninfected, (3) males infected-females uninfected, and (4) males uninfected-females infected, using fecundity measures as response variables. Interactive effects of infection between sexes were prevalent. Uninfected females produced more and heavier eggs when crossed with uninfected than infected males. Uninfected males, in turn, sired more eggs and nymphs when crossed with uninfected than infected females. Unexpectedly, infected males sired more nymphs when crossed with infected than uninfected females. These results can be explained by the effect of parasitism on host body size. As infection reduced size in both genders, infection on one sex only creates body size mismatches and mating constraints that are not present in pairs with the same infection status. Our results indicate the fitness impact of parasitism was contingent on the infection status of genders and mediated by body size. As the fecundity impact of parasitism cannot be estimated independently for each gender, inferences based only on female host infection run the risk of providing biased estimates of parasite-mediated impact on host reproduction.

SUBMITTER: Botto-Mahan C

PROVIDER: S-EPMC5433981 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundTriatoma rubrofasciata is the only kissing bug species distributed globally. In the Americas, this species transmits the parasite Trypanosoma cruzi, responsible for Chagas disease. The presence of T. rubrofasciata in several Asian countries has greatly increased recently. In Vietnam, it is found in large numbers, closely associated with human environments. Although T. rubrofasciata from Asia is not infected with Tryp. cruzi, it carries other parasites such as Trypanosoma lewisi and Trypanosoma conorhini. Reports of bites by T. rubrofasciata have increased significantly in several places of Vietnam, becoming a public health problem as it produces severe anaphylactic reactions.MethodsSpecimens of T. rubrofasciata were collected from seven provinces in central Vietnam. We analyzed different biological attributes (life-cycle, starvation resistance, feeding and reproductive capacities) and genetic characteristics (chromosomes and DNA sequences) of T. rubrofasciata from Vietnam and compared them with Brazilian specimens. Natural infection with Tryp. conorhini and Tryp. lewisi were analyzed in a sample of 100 collected insects.ResultsSpecies identification of T. rubrofasciata from central Vietnam was corroborated by genetic markers. Cytogenetic analyses showed that T. rubrofasciata from central Vietnam share the same chromosomal characteristics with individuals from Brazil and Hanoi. DNA sequence analyses of a mitochondrial cytochrome b gene fragment showed little variation between Old and New World specimens. Our study sample, compared with Brazilian individuals, showed a higher survival capacity revealed by a higher hatching rate (98% compared with 80.5%), a larger amount of blood taken in single meal and long-term starvation resistance. Furthermore, this species had a high natural rate of infection with Tryp. conorhini (46%) and Tryp. lewisi (27%).ConclusionsFor T. rubrofasciata of Vietnam, a high rate of fecundity throughout the year, a high capacity for starvation, and its occurrence in synanthropic environments of urban areas with a high availability of food sources are risk factors to be taken into account by vector control campaigns. The several allergic reactions caused by their bites and their high infection with Tryp. lewisi highlight the need to implement specific control programmes for T. rubrofasciata in Vietnam.

Project description:Due to an abundance of repetitive DNA, the annotation of heterochromatic regions of the genome such as the Y chromosome is problematic. The Y chromosome is involved in key biological functions such as male-fertility and sex-determination and hence, accurate identification of its sequences is vital. The hemipteran insect Rhodnius prolixus is an important vector of Chagas disease, a trypanosomiasis affecting 6-7 million people worldwide. Here we report the identification of the first Y-linked genes of this species.The R. prolixus genome was recently sequenced using separate libraries for each sex and the sequences assembled only with male reads are candidates for Y linkage. We found 766 such candidates and PCR tests with the ten largest ones, confirmed Y-linkage for all of them, suggesting that "separate libraries" is a reliable method for the identification of Y-linked sequences. BLAST analyses of the 766 candidate scaffolds revealed that 568 scaffolds contained genes or part of putative genes. We tested Y-linkage for 36 candidates and found that nine of them are Y-linked (the PCR results for the other 25 genes were inconclusive or revealed autosomal/X-linkage). Hence, we describe in this study, for the first time, Y-linked genes in the R. prolixus genome: two zinc finger proteins (Znf-Y1 and Znf-Y2), one metalloproteinase (Met-Y), one aconitase/iron regulatory protein (Aco-Y) and five genes devoid of matches in any database (Rpr-Y1 to Rpr-Y5). Expression profile studies revealed that eight genes are expressed mainly in adult testis (some of which presented a weak expression in the initial developmental stages), while Aco-Y has a gut-restricted expression.In this study we showed that the approach used for the R. prolixus genome project (separate sequencing of male and female DNA) is key to easy and fast identification of sex-specific (e.g. Y chromosome sequences). The nine new R. prolixus Y-linked genes reported here provide unique markers for population and phylogenetic analysis and further functional studies of these genes may answer some questions about sex determination, male fertility and Y chromosome evolution in this important species.

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Sex-dependent infection causes nonadditive effects on kissing bug fecundity.

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