Differences in Microbiota Between Two Multilocus Lineages of the Sugarcane Aphid (Melanaphis sacchari) in the Continental United States

Abstract

The sugarcane aphid (SCA), Melanaphis Sacchari (Zehntner) (Hemiptera: Aphididae), has been considered an invasive pest of sugarcane in the continental United States since 1977. Then, in 2013, SCA abruptly became a serious pest of U.S. sorghum and is now a sorghum pest in 22 states across the continental United States. Changes in insect-associated microbial community composition are known to influence host-plant range in aphids. In this study, we assessed whether changes in microbiota composition may explain the SCA outbreak in U.S. sorghum. We characterized the SCA bacterial microbiota on sugarcane and grain sorghum in four U.S. states, using a metabarcoding approach. In addition, we used taxon-specific polymerase chain reaction (PCR) primers to screen for bacteria commonly reported in aphid species. As anticipated, all SCA harbored the primary aphid endosymbiont Buchnera aphidicola, an obligate mutualistic bacterial symbiont. Interestingly, none of the secondary symbionts, facultative bacteria typically associated with aphids (e.g., Arsenophonus, Hamiltonella, Regiella) were present in either the metabarcoding data or PCR screens (with the exception of Rickettsiella and Serratia, which were detected by metabarcoding at low abundances <1%). However, our metabarcoding detected bacteria not previously identified in aphids (Arcobacter, Bifidobacterium, Citrobacter). Lastly, we found microbial host-associated differentiation in aphids that seems to correspond to genetically distinct aphid lineages that prefer to feed on grain sorghum (MLL-F) versus sugarcane (MLL-D).

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).…”

Aphid Species Specializing on Milkweed Have Distinct Bacterial Symbiont Communities

“…shows diet breadth is linked to microbiome diversity and community structure [21]. Previous research also indicates the composition of aphid microbial communities are structured by host plant [11,15,16,20,22,24,43,44] and heritable bacterial symbionts are involved in expanding diet breadth [23,25].…”

“…Microbes are also hypothesized to contribute to variation in the capacity of insect herbivores to consume chemically defended plants [8]. Finally, feeding on different host plants can in uence the composition of microbial communities associated with insect herbivores [11,14,19,20]. However, aside from a handful of wellcharacterized nutritional symbionts it is unclear to what extent insect microbial communities either directly or indirectly contribute to host plant adaptation and diet breadth.…”

Host‐associated differentiation of target pests should be assessed before using gene drive as a pest control tool − an opinion

“…Characterizing genetically differentiated populations is not only important for assessing patterns of partial reproductive isolation and therefore gene drive speed of spread, but also because genetically differentiated populations may vary in traits relevant to pest control (Medina, 2012;Araya-Anchetta et al, 2015). For example, genetically differentiated populations have been found to differ in several traits relevant to pest control, such as insecticide resistance (Nauen & Denholm, 2005;Carletto et al, 2010), cold hardiness (Broberg et al, 2018), diapause timing (Boivin et al, 2004;Dambroski & Feder, 2007), number of generations per season (Boivin et al, 2004), host plant resistance (Hanson et al, 2018), host preference (Linn et al, 2003), host range (Feder et al, 1988;Peccoud et al, 2009), vector competence (Boukari et al, 2020), microbiota composition (Medina et al, 2011;Holt et al, 2020), and susceptibility to natural enemies (Hufbauer & Via, 1999;Martinez et al, 2014). Similarly, genetically differentiated pest populations may show different degrees of gene drive resistance.…”