skip to main content


Title: 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.

 
more » « less
NSF-PAR ID:
10449212
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
11
Issue:
20
ISSN:
2045-7758
Page Range / eLocation ID:
p. 14282-14292
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. While low serotonergic activity is often associated with psychological disorders such as depression, anxiety, mood, and personality disorders, variations in serotonin also contribute to normal personality differences. In this study, we investigated the role of blood DNA methylation levels at individual CpG sites of two key serotonergic genes (serotonin receptor gene 1A, HTR1A; serotonin transporter gene, SLC6A4) in predicting the personalities of captive chimpanzees. We found associations between methylation at 9/48 CpG sites with four personality dimensions: Dominance, Reactivity/Dependability, Agreeableness, and Openness. Directionality of effects were CpG location-dependent and confirmed a role of serotonergic methylation in reducing anxiety (Dominance) and aggression-related personality (Reactivity/Undependability) while simultaneously promoting prosocial (Agreeableness) and exploratory personalities (Openness). Although early-life adversity has been shown to impact serotonergic methylation patterns in other species, here, atypical early social rearing experiences only had a modest impact on CpG methylation levels in this chimpanzee sample. The precise environmental factors impacting serotonergic methylation in chimpanzees remain to be identified. Nevertheless, our study suggests a role in shaping natural variation in animal personalities. The results of this study offer a basis for future hypothesis-driven testing in additional populations and species to better understand the impact of ecology and evolution on complex behavioral traits.

     
    more » « less
  2. Abstract

    As animals gain parental experience, they often show more rapid and efficient parental care responses that likely improve offspring survival and fitness. Changes in circulating hormones that underlie reproductive behaviors, including prolactin, have been found to correlate with parental experience in birds and mammals. Altered responsiveness to prolactin in key behavioral centers of the brain may also underlie the effects of experience on parental behaviors. Further, experience may also affect responsiveness to prolactin stimulatory hormones, such as hypothalamic vasoactive intestinal peptide (VIP). While experience has been shown to upregulate neural prolactin receptors and responsiveness in rodents, its effects on prolactin receptor gene expression remain unstudied in birds. To address this, we examined gene expression of pituitary prolactin, hypothalamic prolactin receptors in the preoptic area, hypothalamic VIP, and pituitary VIP receptors in both sexes of the biparental rock dove (Columba livia) when birds were not actively nesting. As age and parental experience are often confounded (i.e.,experienced parents tend to be older than their inexperienced counterparts), we measured gene expression in birds of varying combinations of age (0.6–3 years) and prior reproductive experience (0–12 chicks raised). We found that increasing experience with chicks correlated with lower PRLR expression in the preoptic area, and age correlated with lower VIP expression in birds of both sexes. Pituitary PRL and VIPR expression was not associated with parental experience or age. These results suggest there may be persistent effects of experience and age on neural responsiveness to, and regulation of, prolactin in birds.

     
    more » « less
  3. Abstract

    Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera.

     
    more » « less
  4. Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries. 
    more » « less
  5. Abstract

    Care of infants is a hallmark of mammals. Whereas parental care by mothers is obligatory for offspring survival in virtually all mammals, fathers provide care for their offspring in only an estimated 5%–10% of genera. In these species, the transition into fatherhood is often accompanied by pronounced changes in males’ behavioral responses to young, including a reduction in aggression toward infants and an increase in nurturant behavior. The onset of fatherhood can also be associated with sensory, affective, and cognitive changes. The neuroplasticity that mediates these changes is not well understood; however, fatherhood can alter the production and survival of new neurons; function and structure of existing neurons; morphology of brain structures; and neuroendocrine signaling systems. Although these changes are thought to promote infant care by fathers, very little evidence exists to support this hypothesis; in most cases, neither the mechanisms underlying neuroplasticity in fathers nor its functional significance is known. In this paper, we review the available data on the neuroplasticity that occurs during the transition into fatherhood. We highlight gaps in our knowledge and future directions that will provide key insights into how and why fatherhood alters the structure and functioning of the male brain.

     
    more » « less