Garza, S. F. | bioRxiv Science

bioRxiv2019

Socially dominant, aggressive males are poor influencers of group-consensus in a social fish

In many species, cultures, and contexts, social dominance reflects the ability to exert influence over others, and the question of what makes an effective leader is pertinent to a range of disciplines and contexts. While dominant individuals are often assumed to be most influential, the behavioral traits that make them dominant may also make them socially aversive and thereby reduce their influence. Here we examine the influence of dominant and subordinate males on group behavior in different social contexts using the cichlid fish Astatotilapia burtoni. We find that phenotypically dominant males display behavioral traits that typify leadership across taxonomic systems - aggressive, social centrality, and movement leadership, while subordinate males are passive, socially peripheral, and have little influence over movement. However, in a more complex group-consensus task involving visual cue associations, subordinate males become the most effective agents of social change. We find that dominant males are spatially distant and have lower signal-to-noise ratios of informative behavior in the association task, potentially interfering with their ability to generate group-consensus. In contrast, subordinate males are physically close to other group members, have high signal-to-noise behaviors in the association task, and visual connectivity to other group members equal to that of dominant males. The attributes that define effective social influence are therefore highly context-specific, with socially and phenotypically dominant males being influential in routine but not complex social scenarios. These results demonstrate that behavioral traits that are typical of socially dominant individuals may actually reduce their social influence in other contexts. Significance StatementThe attributes that allow individuals to attain positions of social power and dominance are common across many vertebrate social systems - aggression, intimidation, coercion. Yet these traits are socially aversive, and can make dominant individuals poor agents of social change. In a vertebrate system (social cichlid fish) we show that dominant males are aggressive, socially central, and lead group movement. Yet dominant males are poor effectors of consensus in an more sophisticated association task compared with passive, socially-peripheral subordinate males. The most effective agents of social influence possess behavioral traits opposite of those typically found in position of social dominance, suggesting the behavioral processes that generate social dominance may simultaneously place the most ineffective leaders in positions of power.

animal behavior and cognition↗

bioRxiv2019

A novel terpene synthase produces an anti-aphrodisiac pheromone in the butterfly Heliconius melpomene

Terpenes, a group of structurally diverse compounds, are the biggest class of secondary metabolites. While the biosynthesis of terpenes by enzymes known as terpene synthases (TPSs) has been described in plants and microorganisms, few TPSs have been identified in insects, despite the presence of terpenes in multiple insect species. Indeed, in many insect species, it remains unclear whether terpenes are sequestered from plants or biosynthesised de novo. No homologs of plant TPSs have been found in insect genomes, though insect TPSs with an independent evolutionary origin have been found in Hemiptera and Coleoptera. In the butterfly Heliconius melpomene, the monoterpene (E)-{beta}-ocimene acts as an anti-aphrodisiac pheromone, where it is transferred during mating from males to females to avoid re-mating by deterring males. To date only one insect monoterpene synthase has been described, in Ips pini (Coleoptera), and is a multifunctional TPS and isoprenyl diphosphate synthase (IDS). Here, we combine linkage mapping and expression studies to identify candidate genes involved in the biosynthesis of (E)-{beta}-ocimene. We confirm that H. melpomene has two enzymes that exhibit TPS activity, and one of these, HMEL037106g1 is able to synthesise (E)-{beta}-ocimene in vitro. Unlike the enzyme in Ips pini, these enzymes only exhibit residual IDS activity, suggesting they are more specialised TPSs, akin to those found in plants. Phylogenetic analysis shows that these enzymes are unrelated to previously described plant and insect TPSs. The distinct evolutionary origin of TPSs in Lepidoptera suggests that they have evolved multiple times in insects.\n\nSignificance statementTerpenes are a diverse class of natural compounds, used by both plants and animals for a variety of functions, including chemical communication. In insects it is often unclear whether they are synthesised de novo or sequestered from plants. Some plants and insects have converged to use the same compounds. For instance, (E)-{beta}-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. We describe two novel terpene synthases, one of which synthesises (E)-{beta}-ocimene in H. melpomene, unrelated not only to plant enzymes but also other recently identified insect terpene synthases. This provides the first evidence that the ability to synthesise terpenes has arisen multiple times independently within the insects.

biochemistry↗