Host plant and population source drive diversity of microbial gut communities in two polyphagous insects

Abstract

Symbioses between insects and microbes are ubiquitous, but vary greatly in terms of function, transmission mechanism, and location in the insect. Lepidoptera (butterflies and moths) are one of the largest and most economically important insect orders; yet, in many cases, the ecology and functions of their gut microbiomes are unresolved. We used high-throughput sequencing to determine factors that influence gut microbiomes of field-collected fall armyworm ( Spodoptera frugiperda ) and corn earworm ( Helicoverpa zea ). Fall armyworm midgut bacterial communities differed from those of corn earworm collected from the same host plant species at the same site. However, corn earworm bacterial communities differed between collection sites. Subsequent experiments using fall armyworm evaluating the influence of egg source and diet indicated that that host plant had a greater impact on gut communities. We also observed differences between regurgitant (foregut) and midgut bacterial communities of the same insect host, suggesting differential colonization. Our findings indicate that host plant is a major driver shaping gut microbiota, but differences in insect physiology, gut region, and local factors can also contribute to variation in microbiomes. Additional studies are needed to assess the mechanisms that affect variation in insect microbiomes, as well as the ecological implications of this variability in caterpillars.

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…Our observations are somewhat contrasting with other systems in which nutritionally acquired metabolites of the host plant have been observed to strongly shape the animal gut communities (Koropatkin et al, 2012;Etxeberria et al, 2013;Lu et al, 2014;Xu et al, 2016). Our results also contrast several other studies in insects that have highlighted the importance of host plant in shaping the gut microbiota community (Broderick et al, 2004;Xiang et al, 2006;Pinto-Tomás et al, 2011;Gayatri Priya et al, 2012;Mason and Raffa, 2014;Berman et al, 2018;Jones et al, 2019), including a study of actively feeding late instar stage of M. cinxia (Ruokolainen et al, 2016). The microbiota of actively feeding individuals are evidently affected by the plant material that they feed on, which can lead to rapid and reversible changes in the microbiota community depending on the organic matter, defensive metabolites.…”

“…Our observations are somewhat contrasting with other systems in which nutritionally acquired metabolites of the host plant have been observed to strongly shape the animal gut communities (Koropatkin et al ., ; Etxeberria et al ., ; Lu et al ., ; Xu et al ., ). Our results also contrast several other studies in insects that have highlighted the importance of host plant in shaping the gut microbiota community (Broderick et al ., ; Xiang et al ., ; Pinto‐Tomás et al ., ; Gayatri Priya et al ., ; Mason and Raffa, ; Berman et al ., ; Jones et al ., ), including a study of actively feeding late instar stage of M . cinxia (Ruokolainen et al ., ).…”

Cabbage looper (Trichoplusia ni Hübner) labial glands contain unique bacterial flora in contrast with their alimentary canal, mandibular glands, and Malpighian tubules

“…In terms of the distribution of ASVs among phyla and families of bacteria, the alimentary canal bacteria of T. ni larvae feeding on collards appeared similar to other lepidopteran species (Jones et al, ; Paniagua Voirol, Frago, Kaltenpoth, Hilker, & Fatouros, ). The two most abundant ASVs from the midgut and other organs, apparently belong to the genera Cloacibacterium and Diaphorobacter , members of which have been previously reported from insect gut microbiomes (Montagna et al, ; Ravenscraft, Kish, Peay, & Boggs, ).…”

Gut microbiota metabolic potential correlates with body size between mulberry‐feeding lepidopteran pest species

“…Various studies have shown that abundant microorganisms, particularly bacteria, persist in the larval gut across a range of Lepidoptera species . However, the majority of these studies have focused on structural differences in the bacterial community, with few examining functional variability in bacterial communities across different species within Lepidoptera . For example, Heliconius butterflies have a conserved microbiota dominated by Bacillus , Enterococcus and Enterobacteriaceae, whereas abundant Carnobacterium are observed in the spring webworm and diamondback moth microbiotas …”

“…[15][16][17][18][19] However, the majority of these studies have focused on structural differences in the bacterial community, with few examining functional variability in bacterial communities across different species within Lepidoptera. 20,21 For example, Heliconius butterflies have a conserved microbiota dominated by Bacillus, Enterococcus and Enterobacteriaceae, 22 whereas abundant Carnobacterium are observed in the spring webworm and diamondback moth microbiotas. 23 As a result, we currently do not know how the metabolic capacity of bacterial communities varies as a function of host phylogeny and whether there are predictable patterns driven by the host phenotype within Lepidoptera.…”