Stage- and sex-specific transcriptome analyses reveal distinctive sensory gene expression patterns in a butterfly

Abstract

Background Animal behavior is largely driven by the information that animals are able to extract and process from their environment. However, the function and organization of sensory systems often change throughout ontogeny, particularly in animals that undergo indirect development. As an initial step toward investigating these ontogenetic changes at the molecular level, we characterized the sensory gene repertoire and examined the expression profiles of genes linked to vision and chemosensation in two life stages of an insect that goes through metamorphosis, the butterfly Bicyclus anynana. Results Using RNA-seq, we compared gene expression in the heads of late fifth instar larvae and newly eclosed adults that were reared under identical conditions. Over 50 % of all expressed genes were differentially expressed between the two developmental stages, with 4,036 genes upregulated in larval heads and 4,348 genes upregulated in adult heads. In larvae, upregulated vision-related genes were biased toward those involved with eye development, while phototransduction genes dominated the vision genes that were upregulated in adults. Moreover, the majority of the chemosensory genes we identified in the B. anynana genome were differentially expressed between larvae and adults, several of which share homology with genes linked to pheromone detection, host plant recognition, and foraging in other species of Lepidoptera. Conclusions These results revealed promising candidates for furthering our understanding of sensory processing and behavior in the disparate developmental stages of butterflies and other animals that undergo metamorphosis.

A learning experience elicits sex-dependent neurogenomic responses in Bicyclus anynana butterflies

“…2; S16 Table). Additionally, four genes with putative chemosensory functions were differentially expressed, all of which were upregulated in females relative to males (chemosensory protein 6, BANY.1.2.g12995 ; ejaculatory bulb-specific protein 3-like, BANY.1.2.g12992 ; ejaculatory bulb-specific protein 3-like, BANY.1.2.g12993 ; and odorant receptor Or2-like, BANY.1.2.g25738 ) (Ernst and Westerman, 2021). Finally, a gene encoding vitellogenin-like ( BANY.1.2.g11921 ), a protein known to influence the social behavior of numerous insect species (Morandin et al, 2019; Nelson et al, 2007; Roy-Zokan et al, 2015), was also upregulated in females.…”

“…In both tissues, these sex:condition interactions were found for genes involved with neural development and signaling, and interactions were also found for genes linked to eye development in the eye comparison (S16 Table). In addition, a gene putatively involved with chemoreception (olfactory receptor 21, BANY.1.2.g12009 ; (Ernst and Westerman, 2021)) and a gene associated with regulating circadian rhythms (protein LSM12 homolog, BANY.1.2.g13734 ; (Lee et al, 2017)) showed significant sex:condition interactions in the brain and eyes, respectively.…”

“…ejaculatory bulb-specific protein 3-like, BANY.1.2.g12993; and odorant receptor Or2-like, BANY.1.2.g25738) (Ernst and Westerman, 2021). Finally, a gene encoding vitellogeninlike (BANY.1.2.g11921), a protein known to influence the social behavior of numerous insect species (Morandin et al, 2019;Nelson et al, 2007;Roy-Zokan et al, 2015), was also upregulated in females.…”

“…We might also find differential expression of putative “magic genes,” genes subject to divergent selection that also pleiotropically affect reproductive isolation, potentially by being associated with both the production of and preference for given a trait (Servedio et al, 2011), such as butterfly wing patterning genes. Many wing patterning genes are expressed in the heads of B. anynana (Ernst and Westerman, 2021), and males and females have different wing patterns, with males having brighter UV-reflective eyespots than females (Everett et al, 2012; Prudic et al, 2011) while females have more dorsal hindwing spots than males (Westerman et al, 2014). Additionally, since males but not females produce pheromones that can act as the unconditioned stimuli for learning (Nieberding et al, 2008; Westerman and Monteiro, 2013), we may identify female-specific expression of genes in chemosensory processing pathways.…”

Development of dim-light vision in the nocturnal coral reef fish family, Holocentridae

“…Although whole-retina changes in gene expression have not been studied in teleosts that undergo major ecological shifts, some insights can be gained from other taxa. For example, butterflies show developmental changes in visual gene expression alongside changes in eye structure and therefore, some of the stage-specific expression differences were attributed to cellular composition (Ernst and Westerman 2021). Similarly, since the holocentrid retina underwent cellular remodelling over development, it is likely that some of the expression changes simply facilitate these structural changes.…”