Red Imported Fire Ant (Solenopsis invicta) Chemosensory Proteins Are Expressed in Tissue, Developmental, and Caste-Specific Patterns

Abstract

The red imported fire ant, <i>Solenopsis invicta</i>, is a eusocial invasive insect that has spread worldwide. Chemosensory proteins (CSPs) are ligand-binding proteins that participate in a diverse range of physiological processes that include olfaction and chemical transport. Here, we performed a systematic survey of the expression of the 21 gene <i>S. invicta CSP</i> family that includes at least two groups of apparent <i>S. invicta</i>-specific gene expansions. These data revealed caste, tissue, and developmental stage-specific differential expression of the <i>SiCSPs</i>. In general, moderate to high <i>SiCSP</i> expression was seen in worker antennae and abdomen tissues with lower expression in head/thorax regions. Male and female alates showed high antennal expression of fewer <i>SiCSPs</i>, with the female alate thorax showing comparatively high <i>SiCSP</i> expression. <i>SiCSP</i> expression was lower in male alates tissues compared to workers and female alates, albeit with some highly expressed <i>SiCSPs</i>. <i>SiCSP</i> expression was low during development including in eggs, larvae (early and late instars), and pupae. Global analyses revealed examples of conserved, divergent, and convergent <i>SiCSP</i> expression patterns linked to phylogenetic relationships. The developmental and caste-specific variation seen in <i>SiCSP</i> expression patterns suggests specific functional diversification of CSPs that may translate into differential chemical recognition and communication among individuals and/or reflect other cellular roles of CSPs. Our results support a model for CSPs acting as general ligand carriers involved in a wide range of physiological processes beyond olfaction. As compared to the expression patterns of the <i>S. invicta</i> odorant binding proteins (OBPs), an inverse correlation between <i>SiOBP</i> and <i>SiCSP</i> expression was seen, suggesting potential complementary and/or compensatory functions between these two classes of ligand carriers.