Abstract

The red imported fire ant, Solenopsis invicta, 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 S. invicta CSP family that includes at least two groups of apparent S. invicta-specific gene expansions. These data revealed caste, tissue, and developmental stage-specific differential expression of the SiCSPs. In general, moderate to high SiCSP 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 SiCSPs, with the female alate thorax showing comparatively high SiCSP expression. SiCSP expression was lower in male alates tissues compared to workers and female alates, albeit with some highly expressed SiCSPs. SiCSP expression was low during development including in eggs, larvae (early and late instars), and pupae. Global analyses revealed examples of conserved, divergent, and convergent SiCSP expression patterns linked to phylogenetic relationships. The developmental and caste-specific variation seen in SiCSP 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 S. invicta odorant binding proteins (OBPs), an inverse correlation between SiOBP and SiCSP expression was seen, suggesting potential complementary and/or compensatory functions between these two classes of ligand carriers.

Highlights

  • Ants are the most numerous of the social insects and one of the most successful animals on earth (Holldobler and Wilson, 1990)

  • SiCSP1 showed high similarity (83.7%) to the cuticular hydrocarbon recognition Chemosensory proteins (CSPs) identified in the Japanese carpenter ant (C. japonicus), labeled as C. japonicus CSP1 (CjCSP1) in Figure 1 (Ozaki et al, 2005)

  • Of the general SiCSPs, SiCSPs 3 and 4, SiCSP2, SiCSP8, and SiCSP7 were located on linkage groups (Lg-) 1, 3, 8, and 16 respectively

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Summary

Introduction

Ants are the most numerous of the social insects and one of the most successful animals on earth (Holldobler and Wilson, 1990). Sometime between 1933 and 1945, this ant likely found its way aboard ships carrying exotic fruits, lumber, and other goods from South America apparently establishing somewhere around Mobile, Alabama in the United States, from where it has spread to many other parts of the world (Tschinkel, 2006; Shoemaker et al, 2011) In this respect, S. invicta has demonstrated a remarkable plasticity in environmental adaptations making it one of the most successful invasive animal species on our planet. Male and female reproductive forms are produced seasonally as the colony matures, a process that can take up to 5 years Depending upon their genetic background S. invicta colonies can have one (monogyny) or multiple queens (polygyny) (Ross and Fletcher, 1985; Gotzek and Ross, 2008). Linked to a single gene, termed Gp-9 (renamed OBP3), mono- versus polygyne colony organization appears to be linked to a larger 13 Mb non-recombining “social” chromosomal fragment (∼55% of the chromosome) containing at least 616 open reading frames (Wurm et al, 2011; Wang et al, 2013)

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