Angiosperm to Gymnosperm host‐plant switch entails shifts in microbiota of theWelwitschiabug,Probergrothius angolensis(Distant, 1902)

Abstract

The adaptation of herbivorous insects to new host plants is key to their evolutionary success in diverse environments. Many insects are associated with mutualistic gut bacteria that contribute to the host's nutrition and can thereby facilitate dietary switching in polyphagous insects. However, how gut microbial communities differ between populations of the same species that feed on different host plants remains poorly understood. Most species of Pyrrhocoridae (Hemiptera: Heteroptera) are specialist seed‐feeders on plants in the family Malvaceae, although populations of one species, Probergrothius angolensis, have switched to the very distantly related Welwitschia mirabilis plant in the Namib Desert. We first compared the development and survival of laboratory populations of Pr. angolensis with two other pyrrhocorids on seeds of Welwitschia and found only Pr. angolensis was capable of successfully completing its development. We then collected Pr. angolensis in Namibia from Malvaceae and Welwitschia host plants, respectively, to assess their bacterial and fungal community profiles using high‐throughput amplicon sequencing. Comparison with long‐term laboratory‐reared insects indicated stable associations of Pr. angolensis with core bacteria (Commensalibacter, Enterococcus, Bartonella and Klebsiella), but not with fungi or yeasts. Phylogenetic analyses of core bacteria revealed relationships to other insect‐associated bacteria, but also found new taxa indicating potential host‐specialized nutritional roles. Importantly, the microbial community profiles of bugs feeding on Welwitschia versus Malvaceae revealed stark and consistent differences in the relative abundance of core bacterial taxa that correlate with the host‐plant switch; we were able to reproduce this result through feeding experiments. Thus, a dynamic gut microbiota may provide a means for insect adaptation to new host plants in new environments when food plants are extremely divergent.

Host species identity shapes the diversity and structure of insect microbiota

“…While insect species was the strongest driver of structure and diversity of bacterial communities in this study, diet also showed a significative effect. Several previous studies showed that insect‐associated microbial communities are often shaped by their host's diet, for example in termites (Mikaelyan et al, 2015), aphids (Holt et al, 2020; Wu et al, 2018; Xu et al, 2019, 2020), bugs (Martinez et al, 2019), beetles (Kim et al, 2017), fruit flies (Asimakis et al, 2019; Majumder et al, 2019; Malacrinò et al, 2018; Woruba et al, 2019), soldier flies (Bruno et al, 2019) and ants (Russell et al, 2009). Interestingly, the bacterial communities associated with Phtorimaea operculella varied even according to the plant tissue insects were feeding on (Zheng et al, 2020).…”

Differential Profiles of Gut Microbiota and Metabolites Associated with Host Shift of Plutella xylostella

“…For example, compared with PxR, both PxP-1 and PxP-17 harbored abundant Enterococcaceae. Enterococcaceae can facilitate seed consumption in Harpalus pensylvanicus [ 31 ], reduce gut pH [ 32 ] and increase immunity [ 33 ] in Bombyx mori , provide nutrients for Spodoptera littoralis [ 34 ], and protect lepidopterans from Bacillus thuringiensis [ 35 ]. PxP-17 was associated with a decrease in Lachnospiraceae, which metabolize plant polysaccharides [ 36 ] and reduce graft-versus-host disease mortality [ 37 ].…”

Host species identity shapes the diversity and structure of insect microbiota

“…While insect species was the strongest driver of structure and diversity of bacterial communities in this study, diet also showed a significative effect. Several previous studies showed that insect-associated microbial communities are often shaped by their host's diet, for example in termites (Mikaelyan et al, 2015), aphids (Wu et al, 2018;Xu et al, 2019Xu et al, , 2020Holt et al, 2020), bugs (Martinez et al, 2019), beetles (Kim et al, 2017), fruit flies (Malacrinò et al, 2018;Majumder et al, 2019;Woruba et al, 2019;Asimakis et al, 2019), soldier flies (Bruno et al, 2019) and ants (Russell et al, 2009). Interestingly, the bacterial communities associated with Phtorimaea operculella varied even according to the plant tissue insects were feeding on (Zheng et al, 2020).…”