On the Molecular Basis of Division of Labor in Solenopsis invicta (Hymenoptera: Formicidae) Workers: RNA-seq Analysis

Abstract

The fire ant Solenopsis invicta Buren is an important invasive pest. Among S. invicta workers behavioral changes depend on age where younger ants are nurses and older ants foragers. To identify potential genes associated with this division of labor, we compared gene expression between foragers and nurses by high-throughput sequencing. In total, we identified 1,618 genes significantly differently expressed between nurses and foragers, of which 542 were upregulated in foragers and 1,076 were upregulated in nurses. Several pathways related to metabolism were significantly enriched, such as lipid storage and fatty acid biosynthesis, which might contribute to the division of labor in S. invicta. Several genes involved in DNA methylation, transcription, and olfactory responses as well as resistance to stress were differentially expressed between nurses and foragers workers. Finally, a comparison between previously published microarray data and our RNA-seq data in S. invicta shows 116 genes overlap, and the GO term myofibril assembly (GO: 0030239) were simultaneously significantly enriched. These results advance knowledge of potentially important genes and molecular pathways associated with worker division of labor in S. invicta. We hope our dataset will provide . candidate target genes to disrupt organization in S. invicta as a control strategy against this invasive pest

Oxytocin‐like signaling in ants influences metabolic gene expression and locomotor activity

“…, the nursing area) as compared with the foraging area; 2 ) in nurses of Solenopsis invicta 9 cytochrome P450 4C1 transcripts were found to be down-regulated (69), similar to what we found in IP-KD ants (Supplemental Figs. 8 and 9); and 3 ) isolated, single nurses of Camponotus rufiper exhibit higher locomotor activity as compared with foragers (56).…”

Gene expression is stronger associated with behaviour than with age and fertility in ant workers

“…In ants however, despite the broad correlative evidence for brood carers harbouring more lipid storages than foragers [6–9,14,94,95], clear transcriptomic signatures of nutritional status have so far not been found [30,31]. Only a single study identified lipid storage and fatty acid metabolism to be enriched functions of genes differentially expressed between brood carers and foragers [96]. In that study however, transcriptomes of young brood carers and old foragers were compared.…”

“…However, additional analyses, such as GO enrichment, WGCNA and metabolic pathway comparisons are commonly used and provide valuable insights into broader patterns of gene expression [27,30,31,67,68,75,87,90,96]. Hence, results and conclusions depend on the number and identity of large sets of genes, and partly their FDR values and raw read counts provided as an input.…”

Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers

“…Although the association between age, physiology and behavioural specialization is well documented and widespread across the social Hymenoptera, a consensus on the underlying transcriptomic signatures and expression biases of individual candidate genes linked to worker specialization is lacking. For instance, while the transition from brood care to foraging is associated with a strong reduction in body fat reserves in multiple species (Ament et al, ; Bernadou, Busch, & Heinze, ; Porter & Jorgensen, ; Robinson, Feinerman, & Franks, ; Schulz, Huang, & Robinson, ; Toth, Bilof, Henshaw, Hunt, & Robinson, ; Toth, Kantarovich, Meisel, & Robinson, ; Toth & Robinson, ; Tschinkel, ), behaviour‐specific transcriptomic signatures of nutrition‐related and metabolic processes were found in some studies but not in others (Alaux et al, ; Ament, Corona, Pollock, & Robinson, ; Daugherty, Toth, & Robinson, ; Feldmeyer, Elsner, & Foitzik, ; Khamis et al, ; Manfredini et al, ; Qiu, Zhao, & He, ). Information on nutritional status is conveyed via the target of rapamycin and insulin/insulin‐like signalling (IIS) pathways (Ament et al, ; Maestro, Cobo, & Bellés, ; Morton, Cummings, Baskin, Barsh, & Schwartz, ; Nilsen et al, ; Rodrigues & Flatt, ), which interact with juvenile hormone (JH) and the yolk protein precursor Vitellogenin (Vg) (Libbrecht et al, ).…”

“…The inconsistency across studies in the association between gene expression and worker task choice may reflect species‐specific mechanisms regulating behavioural specialization or differences across studies regarding experimental design. Gene expression patterns associated with behavioural specialization of workers are typically identified by comparing brood carers and foragers that not only differ in behaviour but also in age and fertility (Cardoso‐Júnior et al, ; Feldmeyer et al, ; Ingram et al, ; Johnson & Jasper, ; Khamis et al, ; Manfredini et al, ; Qiu et al, ; Scheiner, Entler, Barron, Scholl, & Thamm, ; Zhao et al, ), two factors that are linked to gene expression (Alaux et al, ; Feldmeyer et al, ; Harrison, Hammond, & Mallon, ; Lucas, Romiguier, & Keller, ; Nilsen et al, ; Whitfield, Cziko, & Robinson, ). Not experimentally controlling for age or fertility (in species with potentially fertile workers) when contrasting brood carer and forager transcriptomes could thus lead to confounded data sets and the identification of transcriptomic patterns being linked to any of the three factors or combinations thereof.…”