Survey of neurotransmitter receptor gene expression into and out of parental care in the burying beetle Nicrophorus vespilloides

Abstract

Understanding the genetic influences of traits of nonmodel organisms is crucial to understanding how novel traits arise. Do new traits require new genes or are old genes repurposed? How predictable is this process? Here, we examine this question for gene expression influencing parenting behavior in a beetle, Nicrophorus vespilloides.Parental care, produced from many individual behaviors, should be influenced by changes of expression of multiple genes, and one suggestion is that the genes can be predicted based on knowledge of behavior expected to be precursors to parental care, such as aggression, resource defense, and mating on a resource. Thus, testing gene expression during parental care allows us to test expectations of this "precursor hypothesis" for multiple genes and traits. We tested for changes of the expression of serotonin, octopamine/tyramine, and dopamine receptors, as well as one glutamate receptor, predicting that these gene families would be differentially expressed during social interactions with offspring and associated resource defense. We found that serotonin receptors were strongly associated with social and aggression behavioral transitions. Octopamine receptors produced a complex picture of gene expression over a reproductive cycle. Dopamine was not associated with the behavioral transitions sampled here, while the glutamate receptor was most consistent with a behavioral change of resource defense/aggression. Our results generate new hypotheses, refine candidate lists for further studies, and inform the genetic mechanisms that are co-opted during the evolution of parent-offspring interactions, a likely evolutionary path for many lineages that become fully social. The precursor hypothesis, while not perfect, does provide a starting point for identifying candidate genes.

The evolutionary demise of a social interaction: social partners differ in the rate at which interacting phenotypes are lost

“…Nevertheless, unexpressed social traits are likely to be lost in the longer-run, either because of costs to plasticity or because mutations can easily accumulate in traits unseen by natural selection (Snell-Rood et al, 2009, 2018). A complex interplay of neurotransmitter receptor gene expression regulates care in Nicrophorus vespilloides (Cunningham et al 2021) and in future work, it would be interesting to investigate the vulnerability of these genes to mutation.…”

Insect homolog of oxytocin/vasopressin associated with parenting of males but not females in a subsocial beetle

“…Complex behaviors like parental care involving extensive parent-offspring interactions and provisioning of food to the offspring evolve through the co-option of existing behaviors and their underlying genetic mechanisms [1][2][3][4]. Gene networks are often robust to changes in individual genes, such that multiple genetic mechanisms may produce the same phenotypes [5][6][7][8]. Thus, it is unclear whether the same genes would be co-opted for parental care across taxa.…”

“…Complex behaviors like parental care evolve through the co-option of existing behaviors and their underlying genetic mechanisms (Tallamy 1984; Cunningham et al 2017; Benowitz et al 2018; Moore and Benowitz 2019). However, gene networks are often robust to changes in individual genes, such that multiple genetic mechanisms may produce the same phenotypes (Manceau et al 2010; Berens et al 2015; Barghi et al 2019; Cunningham et al 2021; Berendzen et al 2022). Thus, it is unclear whether the same genes are co-opted for parental care across taxa.…”