Diversity begets diversity: do parasites promote variation in protective symbionts?

Abstract

Insects commonly possess heritable microbial symbionts that increase their resistance to particular parasites. A diverse community of defensive symbionts may thus provide hosts with effective and specific protection against multiple parasites, although costs might constrain the accumulation of many symbionts. In parallel to the allelic diversity in the MHC complex of the vertebrate immune system, parasite diversity could be the driving force behind symbiont diversity. There is indeed evidence that parasites have the ability to drive frequencies of defensive symbionts in their hosts, and that these symbionts influence parasite communities, but direct evidence that parasite diversity can promote symbiont diversity is still lacking. We provide suggestions to investigate this potential link. Highlights:-Heritable microbes provide insects with effective protection against parasites-Such protective symbionts are diverse, specific and costly-These properties are similar to those of the MHC in the vertebrate immune system-Akin to the MHC, symbiont diversity could be driven by parasite diversity

Interactions among Triatoma sanguisuga blood feeding sources, gut microbiota and Trypanosoma cruzi diversity in southern Louisiana

“…These included Bacteroidales and Clostridales, which were overrepresented in uninfected bugs, Bacillales in bugs infected with TcI, Aeromonadales in bugs infected with TcIV, and Burkhodeliales and Enterobacteriales in bugs infected with TcII/TcV. It is unclear whether it is parasite development in the gut that shapes microbial diversity, or if bacterial species modulate T. cruzi growth in a DTU‐specific manner, and it is likely that bidirectional interactions occur, as observed in other insect parasite/symbionts systems (Hafer & Vorburger, 2019), but the result seems to be a particular microbial community in each bug that is associated with a predominant parasite DTU/strain that will be most likely transmitted. Furthermore, microbial alpha diversity was found to be positively correlated with T. cruzi parasite alpha diversity, at least with one of the indices used, suggesting a possible common driving force for increased microbial diversity.…”

Positive association between the diversity of symbionts and parasitoids of aphids in field populations

“…To our knowledge, this presents the first study explicitly looking at the correlation between symbiont and parasite diversity in the field. However, correlations between immune diversity and parasite diversity have previously been observed in other systems, such as in the major histocompatibility complex (MHC) of vertebrates (e.g., Go€ uy De Bellocq et al 2008, Eizaguirre et al 2011, Minias et al 2020, supporting the idea that protective symbionts could be under similar selection as host immune genes (Hafer and Vorburger 2019).…”

“…In combination, these findings suggest that parasitoids and protective symbionts of aphids may reciprocally promote diversity (see Hafer and Vorburger 2019), which should result in corresponding patterns observable in nature. To obtain data on parasitoid and symbiont species richness and diversity, we collected aphids from the genus Aphis and their parasitoid wasps from different populations in Switzerland and neighboring countries and combined these samples with samples collected previously for other purposes (Vorburger and Rouchet 2016, Vorburger et al 2017).…”

“…The immune system is one of the most diverse components in any living organism and this diversity is a response to the multitude of different parasites and pathogens it has to cope with (e.g., Apanius et al 1997, Ghosh et al 2011). Protective symbionts should be subject to similar selection pressures as a host’s own immune system, and therefore, it seems likely that parasites and pathogens may promote patterns of diversity in protective symbionts and vice versa (Hafer and Vorburger 2019). Aphids are particularly well known for their protective symbionts that provide resistance against parasitoids and fungal pathogens (reviewed by Oliver et al 2014, Vorburger 2014, Guo et al 2017, Vorburger and Perlman 2018).…”

Effects of biodiversity in agricultural landscapes on the protective microbiome of insects – a review

“…A further suggestion that is highly relevant to our proposal is to overcome the selection of resistant aphid/symbiont strains by increasing the diversity of the interacting community. This can be achieved by increasing the genetic diversity of a single parasitoid wasp species (Hafer & Vorburger, ) or by increasing species diversity of the natural enemies. In a greenhouse system such diversity can be achieved through release of specific natural enemy communities.…”