Abstract
Chemical structures of several urinary reproductive pheromones in fish have been identified, and their role in the chemical communication of reproductive condition is well characterized. On the contrary, the role of chemical communication in signalling of social/territorial status in fish is poorly understood. Fathead minnows are an example of a fish species whose life history traits appear conducive to evolution of chemical communication systems that confer information about social/territorial status. Male reproduction in this species is dependent upon their ability to acquire and defend a high quality nesting territory, and to attract a female to the nest. We hypothesized that fathead minnow males use visual and urine-derived chemical cues to signal territorial status. To test this hypothesis, effects of territorial acquisition on male-specific secondary sex characteristics (SSCs) and urine volumes were first assessed. Second, frequencies of male urination in varying social contexts were examined. Finally, nuclear magnetic resonance-based metabolomics was used to identify urinary metabolites that were differentially excreted in the urine of territorial versus non-territorial males. The expression of SSCs, sperm, and urine volumes increased with territory acquisition, and either remained unchanged or decreased in non-territorial males. Frequency of male urination increased significantly in the presence of females (but not males), suggesting that females are the main target of the urinary signals. Territorial and non-territorial males had distinct urinary metabolomic profiles. An unforeseen finding was that one could discern future territorial status of males, based on their initial metabolomic profiles. Bile acids and volatile amines were identified as potential chemical signals of social status in the fathead minnow. The finding that trimethylamine (a fishy smelling volatile amine) may be a social cue is particularly interesting, because it is known to bind trace amine-associated receptors, indicating that these receptors may play role in chemical signalling of social status in fish.
Highlights
Urine is commonly used by both invertebrates and vertebrates as a carrier of a variety of chemosensory signals [1,2]
We observed that the stored urine volume co-varied with the expression of androgen-dependent secondary sexual characteristics, which are good indicators of sexual maturity and social status. Based on these preliminary observations, we developed and tested the following hypotheses: 1) expression of secondary sexual characteristics (SSCs), sperm abundance and stored urine quantity are responsive to territorial status, 2) patterns of urine release are dependent on the social context, and 3) metabolite composition of the urine is linked, and responsive to territorial status
There were no significant differences in the initial lengths of territorial males tested in a non-competitive scenario (TNC) (67.1365.44 mm, mean 6 SEM), territorial males tested in a competitive scenario (T) (69.0766.3 mm), and non-territorial males tested in a competitive scenario (NT) (63.8565 mm)
Summary
Urine is commonly used by both invertebrates and vertebrates as a carrier of a variety of chemosensory signals [1,2]. Female fish are a well-studied chemical communication model, and have been shown to actively use urinary pheromones to communicate reproductive status to their conspecifics [5]. Use of urine-based chemical stimuli for communication of social status, and as a tool for manipulation of an opponent’s intrinsic neural state and behavior has been demonstrated in aquatic invertebrates [9,10], suggesting that this strategy might be used by aquatic vertebrates. Recent studies of the role of chemical communication in social interactions suggest that at least two species of fish, Nile tilapia (Oreochromis mossambicus) and an African cichlid (Astatotilapia burtoni) may use urine to advertise social status amongst conspecific males, and females [11,12,13,14]. Barata et al [13] proposed that an aminosterol-like odorant in the urine of male Nile tilapia is used to communicate a male’s social dominance to females, but the exact identities of the chemicals involved in communicating social status in fish remain poorly elucidated
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