skip to main content


Title: Neurogenomic landscape associated with status‐dependent cooperative behaviour
Abstract

The neurogenomic mechanisms mediating male–male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species (Pipra filicauda) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non‐territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision‐making network (SDMN), and two key endocrine tissues that regulate social behaviour. We associated gene expression with each bird's behavioural and endocrine profile derived from 3 years of repeated measures taken from free‐living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex‐steroid and neuropeptide signalling appeared to be important in mediating status‐specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN‐wide gene expression differences between territorial and floater males that could form the basis of ‘status‐specific’ neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems‐level insights into the mechanisms of cooperative behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour.

 
more » « less
NSF-PAR ID:
10496432
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Abstract Differences in social status are often mediated by agonistic encounters between competitors. Robust literature has examined social status-dependent brain gene expression profiles across vertebrates, yet social status and reproductive state are often confounded. It has therefore been challenging to identify the neuromolecular mechanisms underlying social status independent of reproductive state. Weakly electric fish, Gymnotus omarorum , display territorial aggression and social dominance independent of reproductive state. We use wild-derived G. omarorum males to conduct a transcriptomic analysis of non-breeding social dominance relationships. After allowing paired rivals to establish a dominance hierarchy, we profiled the transcriptomes of brain sections containing the preoptic area (region involved in regulating aggressive behaviour) in dominant and subordinate individuals. We identified 16 differentially expressed genes (FDR < 0.05) and numerous genes that co-varied with behavioural traits. We also compared our results with previous reports of differential gene expression in other teleost species. Overall, our study establishes G. omarorum as a powerful model system for understanding the neuromolecular bases of social status independent of reproductive state. 
    more » « less
  2. Abstract

    Selective logging is the primary cause of tropical forest degradation and is rapidly expanding worldwide. While the impacts of logging on species diversity and distributions are well understood, little is known about the effects of logging on animal behaviours central to individual fitness and population persistence.

    The song rate of breeding songbirds is a behavioural trait that is often positively associated with male density and used by conspecific females as an indicator of territory and male quality. Thus, contrasting logging‐induced adjustments in song rates of individual birds with population shifts may illuminate potential mechanisms underlying population distributions.

    We present a novel application of bioacoustic monitoring, integrating counts of individuals, songs and duets from single automated recording units (ARUs) withN‐mixture models, to estimate shifts in population parameters (occupancy, abundance) and singing behaviours (per‐capita song rates, per‐pair duet rates) of 32 Bornean songbird species with logging. We tested hypotheses on the relationships between adjustments in behavioural and population parameters with logging, and further tested the extent to which species traits predicted behavioural and population shifts.

    Adjustments to singing behaviour in 59 and 53% of species (57% of duetting species) were concordant with differences in occupancy and abundance respectively, such that species showing reduced populations with logging also produced fewer songs per‐capita, and vice versa. Species known to prefer undisturbed habitats and large‐bodied species showed the most negative effects of logging on singing behaviour and population distributions. Species known to exploit degraded habitats exhibited the opposite pattern. Subdued singing in logged forests by species of conservation concern suggests limited competition between territorial males in small populations and may also signal low‐quality territories.

    Synthesis and applications. We demonstrate that bioacoustic monitoring can be used to not only estimate important population parameters of occupancy and abundance across a diverse tropical songbird community, but also enables quantification of behaviours considered relevant to individual fitness, yet unobtainable with conventional methods (e.g. point counts). Bioacoustics provides a viable approach to reliable automated large‐scale monitoring of hyperdiverse tropical forest systems under logging operations and other land‐use pressures.

     
    more » « less
  3. null (Ed.)
    Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman ( Porichthys notatus ) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioural tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioural tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behaviour. Our results reveal that divergent expression patterns in a conserved neuroendocrine centre known to regulate social-reproductive behaviours across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics. 
    more » « less
  4. 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
  5. Members of the avian family Pipridae (manakins) have served as a model system for studies aimed at understanding cooperation among individuals, traits involved in sexual selection and the evolution of female preferences. These studies rely on a detailed natural history baseline, yet multiple manakin taxa remain unstudied, precluding comparative analyses and assessment of geographical variation. The Blue‐backed ManakinChiroxiphia pareolais a widely distributed species with four recognized subspecies; however, most published information on display behaviour, social organization and vocalizations are derived from an island population of one subspecies,Chiroxiphia pareola atlantica. To describe the social organization and patterns of activity of the subspeciesC. p. napensis,we studied a population in eastern Ecuador and collected data from seven display areas or leks within the Tiputini Biodiversity Station. We used focal observations, camera traps and automatic song recorders to collect information for the field seasons from January to March 2013 and video cameras from February to March 2014. Males were active most of the day with a peak in activity at noon. Display areas were occupied by one to five males, ranging from > 2 to > 18 years old. The vocal repertoire included duet song displays and a variety of calls. We provide sonograms for all six observed vocalizations, including two previously unrecorded vocalizations for the species, and comment on the possible behavioural context of each vocalization. We describe five distinct display elements and the dance display behaviour, and highlight differences relative to other species of the genus. The first part of the dance display involved cooperative dancing, whereas the second part was a solo display, usually performed by alpha males. Our work reveals some differences betweenC. p. napensisandC. p. atlantica,such as a possible aggressive interaction between males of different ages and hierarchical status that has not been reported before and the apparent absence of mechanical wing sounds inC. p. napensis. The data reported here help advance our knowledge of the evolution of display behaviour among manakins.

     
    more » « less