Analysis of natural female post-mating responses of Anopheles gambiae and Anopheles coluzzii unravels similarities and differences in their reproductive ecology

Thailayil, Janis; Gabrieli, Paolo; Caputo, Beniamino; Bascuñán, Priscila; South, Adam; Diabaté, Abdoulaye; Dabiré, Roch K.; Torre, Alessandra della; Catteruccia, Flaminia

doi:10.1038/s41598-018-24923-w

Cited by 19 publications

(30 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Reproductive isolation between A. coluzzii and A. gambiae appears to be mediated mostly by premating mechanisms; however, recent reports that assortative mating is “leaky” (Lee, Marsden, et al, ) suggest that species boundaries are maintained by postmating mechanisms as well. The large number of A. gambiae ‐specific SNPs present in the genomes of backcrossed individuals and the relatively gradual decrease in the frequency of some introgressed SNPs support the observation that postmating reproductive isolation between A. coluzzii and A. gambiae in nature is postzygotic, arising from unfit hybrid genotypes, as suggested by Lee, Marsden, et al () and Pombi et al (), and not prezygotic as suggested by Thailayil et al (), in which case hybrid genotypes would be absent altogether.…”

Section: Discussionsupporting

confidence: 70%

The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population

et al. 2018

View full text Add to dashboard Cite

Animal species are able to acquire new genetic material via hybridization and subsequent introgression. However, little is known about how foreign genomic material is incorporated into a population over time and what genes are susceptible to introgression. Here, we follow the closely related mosquito sister species Anopheles coluzzii and Anopheles gambiae in a sympatric natural population in Mali at multiple time points spanning a period of 25 years. During this period, we observed the temporary breakdown of mating barriers, which allowed us to explore the fate of alleles that crossed the species boundary in a natural population. Whole genome sequencing of 74 individuals revealed introgression within only 34 genes (0.26% of total genes) from A. gambiae to A. coluzzii, the majority contained within a 4 Mb region on the 2L chromosome which includes the insecticide resistance gene (AGAP004707). We designed a genotyping assay to follow 25 of the 34 introgressed alleles over time and found that all A. gambiae alleles, except four, reached a frequency of 50% in the A. coluzzii population within 4 years (~50 generations) and increased to ~80% within 6 years (~75 generations). However, the frequency of all introgressed alleles, except three, decreased to ~60% in 2016. This suggests an ongoing process of purifying selection in the population against DNA of foreign ancestry, except for alleles that are under positive selection, resulting in a complex genomic landscape. This study shows that stable introgression is limited to only specific genes even within closely related species.

show abstract

Section: Discussionsupporting

confidence: 70%

The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population

et al. 2018

View full text Add to dashboard Cite

show abstract

“…gambiae and An . coluzzii [14]. These differences will need further exploration to better understand if the results we present found here for An .…”

Section: Discussionmentioning

confidence: 80%

“…gambiae and An . coluzzii post-transcriptional responses in the lower reproductive tract and carcass have been observed, in particular with genes involved in reproduction and immunity [14]. For example, the important immune gene TEP1 is only found to be significantly upregulated in An .…”

Section: Introductionmentioning

confidence: 99%

The male mosquito contribution towards malaria transmission: Mating influences the Anopheles female midgut transcriptome and increases female susceptibility to human malaria parasites

et al. 2019

View full text Add to dashboard Cite

Mating causes dramatic changes in female physiology, behaviour, and immunity in many insects, inducing oogenesis, oviposition, and refractoriness to further mating. Females from the Anopheles gambiae species complex typically mate only once in their lifetime during which they receive sperm and seminal fluid proteins as well as a mating plug that contains the steroid hormone 20-hydroxyecdysone. This hormone, which is also induced by blood-feeding, plays a major role in activating vitellogenesis for egg production. Here we show that female Anopheles coluzzii susceptibility to Plasmodium falciparum infection is significantly higher in mated females compared to virgins. We also find that mating status has a major impact on the midgut transcriptome, detectable only under sugar-fed conditions: once females have blood-fed, the transcriptional changes that are induced by mating are likely masked by the widespread effects of blood-feeding on gene expression. To determine whether increased susceptibility to parasites could be driven by the additional 20E that mated females receive from males, we mimicked mating by injecting virgin females with 20E, finding that these females are significantly more susceptible to human malaria parasites than virgin females injected with the control 20E carrier. Further RNAseq was carried out to examine whether the genes that change upon 20E injection in the midgut are similar to those that change upon mating. We find that 79 midgut-expressed genes are regulated in common by both mating and 20E, and 96% (n = 76) of these are regulated in the same direction (up vs down in 20E/mated). Together, these findings show that male Anopheles mosquitoes induce changes in the female midgut that can affect female susceptibility to P. falciparum. This implies that in nature, males might contribute to malaria transmission in previously unappreciated ways, and that vector control strategies that target males may have additional benefits towards reducing transmission.

show abstract

“…Combined with the finding that MISO is highly induced by mating in An. coluzzii females collected from natural mating swarms in the same villages in Burkina Faso [42], our results reveal that this female protein has an important function for maintaining reproductive fitness of field malaria vectors during P. falciparum infection.…”

Section: Discussionmentioning

confidence: 56%

A mating-induced reproductive gene promotesAnophelestolerance toPlasmodium falciparuminfection

Marcenac

Shaw

Kakani

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Anopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin and mated females of two important vectors, Anopheles gambiae and Anopheles stephensi, is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict reproductive costs to their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors.

show abstract

Analysis of natural female post-mating responses of Anopheles gambiae and Anopheles coluzzii unravels similarities and differences in their reproductive ecology

Cited by 19 publications

References 87 publications

The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population

The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population

The male mosquito contribution towards malaria transmission: Mating influences the Anopheles female midgut transcriptome and increases female susceptibility to human malaria parasites

A mating-induced reproductive gene promotesAnophelestolerance toPlasmodium falciparuminfection

Contact Info

Product

Resources

About