TY - JOUR
T1 - Development of Common Leaf-Footed Bug Pests Depends on the Presence and Identity of Their Environmentally Acquired Symbionts
AU - Hunter, Martha S.
AU - Umanzor, Edwin F.
AU - Kelly, Suzanne E.
AU - Whitaker, Shaira Marie
AU - Ravenscraft, Alison
N1 - Publisher Copyright:
Copyright © 2022 American Society for Microbiology. All Rights Reserved.
PY - 2022/3
Y1 - 2022/3
N2 - Many beneficial symbioses between bacteria and their terrestrial arthropod hosts are vertically transmitted from mother to offspring, ensuring that the progeny acquire necessary partners. Unusually, in several families of coreoid and lygaeoid bugs (Hemiptera), nymphs must instead ingest the beneficial symbiont, Burkholderia (sensu lato), from the environment early in development. We studied the effects of Burkholderia on development of two species of leaf-footed bug (Coreidae) in the genus Leptoglossus, Leptoglossus zonatus and Leptoglossus phyllopus. We found no evidence for vertical transmission of the symbiont but found stark differences in performance between symbiotic and aposymbiotic individuals. Symbiotic nymphs grew more rapidly, were approximately four times more likely to survive to adulthood than aposymbiotic bugs, and were two times larger. These findings suggest that Burkholderia is an obligate symbiont for the Leptoglossus species. We also tested for variation in fitness effects conferred by four symbiont isolates representing different species within the Burkholderia insect-associated stinkbug beneficial and environmental (SBE) clade. While three isolates conferred similar benefits to hosts, nymphs associated with the fourth isolate grew more slowly and weighed significantly less as adults. The effects of the four isolates were similar for both Leptoglossus species. This work indicates that both Burkholderia acquisition and isolate identity play critical roles in the growth and development of Leptoglossus. IMPORTANCE Leptoglossus zonatus and L. phyllopus are important polyphagous pests, and both species have been well-studied but generally without regard to their dependance on a bacterial symbiont. Our results indicate that the central role of Burkholderia in the biology of these insects, as well as in other leaf-footed bugs, should be considered in future studies of coreid life history, ecology, and pest management. Our work suggests that acquisition of Burkholderia is critical for the growth and development of Leptoglossus species. Further, we found that there was variation in performance outcomes according to symbiont identity, even among members of the stinkbug beneficial and environmental clade. This suggests that although environmental acquisition of a symbiont can provide extraordinary flexibility in partner associations, it also carries a risk if the partner is suboptimal.
AB - Many beneficial symbioses between bacteria and their terrestrial arthropod hosts are vertically transmitted from mother to offspring, ensuring that the progeny acquire necessary partners. Unusually, in several families of coreoid and lygaeoid bugs (Hemiptera), nymphs must instead ingest the beneficial symbiont, Burkholderia (sensu lato), from the environment early in development. We studied the effects of Burkholderia on development of two species of leaf-footed bug (Coreidae) in the genus Leptoglossus, Leptoglossus zonatus and Leptoglossus phyllopus. We found no evidence for vertical transmission of the symbiont but found stark differences in performance between symbiotic and aposymbiotic individuals. Symbiotic nymphs grew more rapidly, were approximately four times more likely to survive to adulthood than aposymbiotic bugs, and were two times larger. These findings suggest that Burkholderia is an obligate symbiont for the Leptoglossus species. We also tested for variation in fitness effects conferred by four symbiont isolates representing different species within the Burkholderia insect-associated stinkbug beneficial and environmental (SBE) clade. While three isolates conferred similar benefits to hosts, nymphs associated with the fourth isolate grew more slowly and weighed significantly less as adults. The effects of the four isolates were similar for both Leptoglossus species. This work indicates that both Burkholderia acquisition and isolate identity play critical roles in the growth and development of Leptoglossus. IMPORTANCE Leptoglossus zonatus and L. phyllopus are important polyphagous pests, and both species have been well-studied but generally without regard to their dependance on a bacterial symbiont. Our results indicate that the central role of Burkholderia in the biology of these insects, as well as in other leaf-footed bugs, should be considered in future studies of coreid life history, ecology, and pest management. Our work suggests that acquisition of Burkholderia is critical for the growth and development of Leptoglossus species. Further, we found that there was variation in performance outcomes according to symbiont identity, even among members of the stinkbug beneficial and environmental clade. This suggests that although environmental acquisition of a symbiont can provide extraordinary flexibility in partner associations, it also carries a risk if the partner is suboptimal.
KW - Burkholderia
KW - Gut symbionts
KW - Horizontal transmission
KW - Host-symbiont interactions
KW - Symbiosis
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U2 - 10.1128/aem.01778-21
DO - 10.1128/aem.01778-21
M3 - Article
C2 - 34986009
AN - SCOPUS:85126072709
SN - 0099-2240
VL - 88
JO - Applied and environmental microbiology
JF - Applied and environmental microbiology
IS - 5
M1 - e01778
ER -