Molecular mechanisms and evolutionary implications of social plasticity

Funder

Organizational Unit

Publications

Birth date predicts alternative life-history pathways in a fish with sequential reproductive tactics

Publication . Fagundes, Teresa; Simões, Mariana G.; L. Saraiva, João; Ros, Albert F. H.; Gonçalves, David; Oliveira, Rui F.

1. In species with plastic expression of alternative reproductive tactics (ARTs), individuals of the same sex, usually males, can adopt different reproductive tactics depending on factors such as body size. 2. The 'birth date hypothesis' proposes that condition-dependent expression of ARTs may ultimately depend on birth date, because individuals born at different times of the year may achieve different sizes and express different reproductive tactics accordingly. However, this has rarely been tested. 3. Here, we tested this hypothesis in a fish with ARTs, the peacock blenny (Salaria pavo). A long-term (6 years) mark-recapture study demonstrated that ARTs in the peacock blenny were sequential and that males may follow at least two alternative life-history pathways: a nestholder pathway, in which males express the nest-holder tactic from their first breeding season onwards, and a parasitic pathway, where males reproduce on their first breeding season as sneaker males and subsequently as nest-holders. 4. We have found evidence of a birth date effect on the expression of ARTs in the peacock blenny. Males following the nest-holder pathway are born earlier and are larger at the first breeding season than males following the parasitic pathway, but they have similar growth curves. 5. The mechanisms underlying a birth date effect are far from clear and might be diverse. We have not found support for a mechanism of body size threshold triggering sexual maturation and subsequent ARTs. A mechanism of tactic determination that is strictly based on timing of first maturation is also unlikely. 6. A proxy of lifetime reproductive success shows crossing (body size associated) fitness curves for the two main life-history pathways.

2015-12Journal article

Open access

Social odors conveying dominance and reproductive information induce rapid physiological and neuromolecular changes in a cichlid fish

Publication . Simões, José M.; Barata, Eduardo Nuno; Harris, Rayna M.; O'Connell, Lauren A.; Hofmann, Hans A.; Oliveira, Rui F.

Background: Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and this ability has an impact in their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. Results: We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Conclusions: Our results show that different olfactory stimuli from conspecifics' have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioral plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment.

2015-02Journal article

Open access

RNA-SEQ applied to the peacock blenny Salaria pavo: unveiling the gene networks and signalling pathways behind phenotypic plasticity in a littoral fish

Publication . Cardoso, Sara de Jesus Dias; Canário, Adelino V. M.; Oliveira, Rui Filipe Nunes Pais de

Phenotypic plasticity is the ability of an individual genome to produce different phenotypes depending on environmental cues. These plastic responses rely on diverse genomic mechanisms and allow an organism to maximize its fitness in a variety of social and physical settings. The development of next-generation sequencing (NGS) technologies, especially RNA Sequencing (RNA-Seq), has made it possible to investigate the distinct patterns of gene expression known to be underlying plastic phenotypes in species with ecological interest. In teleost fishes, changes in phenotypes is often observed during the reproductive season, with shifts and adjustments in dominance status that can lead to the co-existence of multiple reproductive morphs within the same population. One such example is the peacock blenny Salaria pavo (Risso, 1810), a species where the intensity of mating competition varies among populations due to nest-site availability, such that two different levels of plasticity arise: 1) intraspecific variation in reproductive behaviour for males that can follow either of two developmental pathways, grow directly into nest-holder males, or behave first as female mimics to sneak fertilizations (sneaker males) and later transition into nest-holder males, and 2) inter-population variation in courting roles of females and nest-holder males. This system provides the ideal basis to apply RNA-Seq methods to study plasticity since differences in reproductive traits within and among populations can reveal which genetic and genomic mechanisms underpin the observed variation in behavioural response to changes in the social environment. However, the genomic information available for this species was scarce, and hence multiple sequencing techniques were used and the methodologies applied optimized throughout the work. In this thesis, we start by first obtaining a de novo transcriptome assembly to develop the first genetic markers for this species (Chapter 2). These microsatellites were used to elucidate the reproductive success (i.e. consisting of mating success and fertilization success) of male ARTs, which can be used as a proxy of Darwinian fitness (Chapter 3). In this study, we detected a fertilization success for nestholder males of 95%, and showed a stronger influence of the social environment rather than morphological variables in the proportion of lost fertilizations by nest-holder males of this species. Taking advantage of the developed transcriptome, we used highthroughput sequencing to obtain expression profiles for male morphs (i.e. intraspecific variation) and females in this species, and focus on the role of differential gene expression in the evolution of sequential alternative reproductive tactics (ARTs) that involve the expression of both male and female traits (Chapter 4). Additionally, we show how the distinct behavioural repertoires are facilitated by distinct neurogenomic states, which discriminate not only sex but also male morphs. Lastly, using two different target tissues, gonads and forebrain, we focus on the genomic regulation of sex roles in courtship behaviour between females and males from two populations under different selective regimes (inter-population variation), the Portuguese coastal population with reversed sex roles and the rocky Italian population with ‘conventional’ sex roles (Chapter 5). Here we demonstrate that variation in gene expression at the brain level segregates individuals by population rather than by sex, indicating that plasticity in behaviour across populations drives variation in neurogenomic expression. On the other hand, at the gonad level, variation in gene expression segregates individuals by sex and then by population, indicating that sexual selection is also acting at the intrasexual level, particularly in nestholder males by paralleling differences in gonadal investment. However, the genomic mechanisms underlying courtship behaviour were not fully elucidated, and more studies are necessary.

2019-05-06Doctoral thesis

Open access