An official website of the United States government
Abstract Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve.In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high‐ or low‐predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity.High‐predation males learned their mating tactic from conspecific adults as juveniles, while low‐predation males did not. High‐predation males increased courtship when exposed to chemical predator cues during development; low‐predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development.Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not.We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.
more »
« less
Behavioural tactic predicts preoptic-hypothalamic gene expression more strongly than developmental morph in fish with alternative reproductive tactics
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
- PAR ID:
- 10274982
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 285
- Issue:
- 1871
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20172742
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Historical data suggest that many bee species have declined in body size. Larger‐bodied bees with narrow phenological and dietary breadth are most prone to declines in body size over time. This may be especially true in solitary, desert‐adapted species that are vulnerable to climate change such asCentris pallida(Hymenoptera: Apidae). In addition, body size changes in species with size‐linked behaviours could threaten the prevalence of certain behavioural phenotypes long‐term.C. pallidasolitary bees are found in the Sonoran Desert. Males use alternative reproductive tactics (ARTs) and are dimorphic in both morphology and behaviour.C. pallidamale body size has been studied since the 1970s in the same population. The authors collected body size data in 2022 and combined it with published records from 1974–2022. The authors find a persistent decline in the mean head width of patrolling males, and shifts towards smaller body sizes in the populations of males found foraging and hovering. Both morphs declined in average body size, and the proportion of large‐morph males in the population decreased by 8%. Mating males did not decline in mean body size over the last five decades. The authors discuss hypotheses related to the decline inC. pallidamale head width. Finally, the authors advocate forC. pallidaas an excellent study system for understanding the stability of ARTs with size‐linked behavioural phenotypes.more » « less
-
In many species, establishing and maintaining a territory is critical to survival and reproduction, and an animal's ability to do so is strongly influenced by the presence and density of competitors. Here we manipulate social conditions to study the alternative reproductive tactics displayed by genetically identical, age-matched laboratory mice competing for territories under ecologically realistic social environmental conditions. We introduced adult males and females of the laboratory mouse strain C57BL/6J into a large, outdoor field enclosure containing defendable resource zones under one of two social conditions. We first created a low-density social environment, such that the number of available territories exceeded the number of males. After males established stable territories, we introduced a pulse of intruder males and observed the resulting defensive and invasive tactics employed. In response to this change in social environment, males with large territories invested more in patrolling but were less effective at excluding intruder males as compared with males with small territories. Intruding males failed to establish territories and displayed an alternative tactic featuring greater exploration as compared with genetically identical territorial males. Alternative tactics did not lead to equal reproductive success—males that acquired territories experienced greater survival and had greater access to females.more » « less
-
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
-
null (Ed.)Males that exhibit alternative reproductive tactics (ARTs) often differ in the risk of sperm competition and the energetic trade-offs they experience. The resulting patterns of selection could lead to between-tactic differences in ejaculate traits. Despite extensive research on male ARTs, there is no comprehensive review of whether and what differences in sperm traits exist between male ARTs. We review existing theory on ejaculate evolution relevant to ARTs and then conduct a comprehensive vote-counting review of the empirical data comparing sperm traits between males adopting ARTs. Despite the general expectation that sneaker males should produce sperm that are more competitive (e.g. higher quality or performance), we find that existing theory does not predict explicitly how males adopting ARTs should differ in sperm traits. The majority of studies find no significant difference in sperm performance traits between dominant and sneaker males. However, when there is a difference, sneaker males tend to have higher sperm performance trait values than dominant males. We propose ways that future theoretical and empirical research can improve our understanding of the evolution of ejaculate traits in ARTs. We then highlight how studying ejaculate traits in species with ARTs will improve our broader knowledge of ejaculate evolution. This article is part of the theme issue ‘Fifty years of sperm competition’.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1098/rspb.2017.2742
