Marion Mehlis

Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues

The ability to recognise kin has been demonstrated in several animal species. However, the mechanisms of kin recognition often remain unknown. The most frequently discussed sensory modalities to recognise kin are visual, olfactory and acoustical cues. Three-spined sticklebacks (Gasterosteus aculeatus) are able to differentiate between kin and non-kin when presented visual and olfactory cues combined. To elucidate, which cues they use to recognise kin female sticklebacks were given the choice between two identical computer animations of courting stickleback males. Next to one animation, water conditioned by a brother was added, while near the other, water from an unrelated male was added. In half of the experiments, the brother was familiar while in the other half he was unfamiliar to the female. Both scenarios were carried out with both outbred and inbred fish. The results showed that the females adjusted their choice behaviour according to relatedness. Furthermore, they were able to recognise both familiar as well as unfamiliar brothers. Inbreeding did not affect this ability. Hence, three-spined sticklebacks are able to recognise their relatives using olfactory cues alone. The cognitive mechanisms underlying this ability were independent from familiarity and not impaired by inbreeding.

To eat or not to eat: egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism

Filial cannibalism occurs in many animal species ranging from insects to mammals, and is especially well described in teleost fishes. Numerous causes may lead to this behaviour, e.g. certainty of paternity. However, the cues males use to assess their paternity often remain unknown. One possible way to differentiate between own and foreign offspring is by using egg cues. Nevertheless, in egg-laying species, evidence for this is still scarce. In this study, male three-spined sticklebacks (Gasterosteus aculeatus), a fish with paternal care in which sneaking as well as filial cannibalism is common, were allowed to care for manipulated nests that contained different percentages of own fertilized eggs. After 7 days, embryo survival was determined. Furthermore, brood-caring as well as aggressive behaviour was measured daily. Clutches containing a higher proportion of foreign eggs were more likely to be completely cannibalized than clutches containing a lower proportion of foreign eggs, particularly when the clutch was laid early in the breeding season. However, the behavioural observations revealed no influence of paternity. The results show that paternity triggers filial cannibalism in sticklebacks and that males are able to evaluate their paternity using egg cues alone.

Shoaling decisions in three-spined sticklebacks (Gasterosteus aculeatus)—familiarity, kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.

Costly plastic morphological responses to predator specific odour cues in three-spined sticklebacks (Gasterosteus aculeatus)

Predation risk is one of the major forces affecting phenotypic variation among and within animal populations. While fixed anti-predator morphologies are favoured when predation level is consistently high, plastic morphological responses are advantageous when predation risk is changing temporarily, spatially, or qualitatively. Three-spined sticklebacks (Gasterosteus aculeatus) are well known for their substantial variability in morphology, including defensive traits. Part of this variation might be due to phenotypic plasticity. However, little is known about sticklebacks’ plastic ability to react morphologically to changing risks of predation and about the proximate cues involved. Using a split-clutch design we show that odour of a predatory fish induces morphological changes in sticklebacks. Under predation risk, i.e., when exposed to odour of a predator, fish grew faster and developed a different morphology, compared to fish reared under low predation risk, i.e., exposed to odour of a non-predatory fish, or in a fish-free environment. However, fast growing comes at cost of increased body asymmetries suggesting developmental constraints. The results indicate that sticklebacks are able to distinguish between predatory and non-predatory fishes by olfactory cues alone. As fishes were fed on invertebrates, this reaction was not induced by chemical cues of digested conspecifics, but rather by predator cues themselves. Further, the results show that variation in body morphology in sticklebacks has not only a strong genetical component, but is also based on plastic responses to different environments, in our case different predation pressures, thus opening new questions for this model species in ecology and evolution.

Nutritional benefits of filial cannibalism in three-spined sticklebacks (Gasterosteus aculeatus)

Although filial cannibalism (eating one’s own offspring) occurs in numerous species, including several teleost fishes, its adaptive value is still not well understood. One often-discussed explanation is that individuals enhance their mass and body condition by consuming part of their eggs. However, evidence for this assumption is scarce thus far. In this study, male three-spined sticklebacks (Gasterosteus aculeatus), a species with paternal care, were allowed to care for a batch of eggs or for an empty nest under food-deprived conditions. All brood-caring males cannibalised at least part of their eggs and thus preserved their initial mass and body condition. Furthermore, mass as well as body condition was significant positively correlated with the number of cannibalised eggs. In contrast, empty-nest males that had no possibility to cannibalise eggs significantly lost mass and body condition. This is, to our knowledge, the first experimentally documented evidence that mass as well as body condition were preserved by filial cannibalism.

Predator‐inspection behaviour in female three‐spined sticklebacks Gasterosteus aculeatus is associated with status of gravidity

Differences in predator-inspection behaviour between gravid and non-gravid female as well as between male and female three-spined sticklebacks Gasterosteus aculeatus were investigated. Gravid females confronted with a live rainbow trout Oncorhynchus mykiss showed bolder inspection behaviour than non-gravid ones. The behaviour of gravid females was comparable with that of males, maybe because both face a high risk of predation. The results indicate that antipredator behaviour in female G. aculeatus is not fixed but adjusted to their reproductive state.

Quantification acuity in spontaneous shoaling decisions of three-spined sticklebacks

The ability to discriminate between different quantities is widespread throughout the animal kingdom, and the underlying mechanisms of quantity discrimination are currently intensely discussed. In contrast, questions elucidating the limits of quantity estimation received rather little attention so far. Here, we examined fine-tuned quantity estimation in the three-spined stickleback (Gasterosteus aculeatus) in a natural context, i.e. during shoaling decisions. Wild-caught focal fish were given the spontaneous choice between two shoals which differed in group size by 1 fish (0 vs. 1, 1 vs. 2, 2 vs. 3, 3 vs. 4, 4 vs. 5, 5 vs. 6 and 6 vs. 7), based on visual assessment. The results show that sticklebacks generally prefer to shoal with the larger group. They discriminated numerical contrasts up to 6 versus 7, equalling a numerical ratio of 0.86. Preference patterns followed Weber’s law, i.e. decreased with increasing numerical ratio. This pattern was found across all numerical conditions as well as within the small number range (ranging from 1 vs. 2 to 3 vs. 4). The results suggest that wild-caught three-spined sticklebacks are spontaneously able (i.e. without prior learning) to detect subtle differences in shoal sizes. Further, they confirm findings of previous studies highlighting the contribution of the analogue magnitude system to quantity estimation in fishes.

Dynamic resource allocation between pre- and postcopulatory episodes of sexual selection determines competitive fertilization success.

In polyandrous mating systems, male reproductive success depends on both mate-acquisition traits (precopulatory) and sperm competitive abilities (postcopulatory). Empirical data on the interaction between these traits are inconsistent; revealing positive, negative or no relationships. It is generally expected that the investment in pre- and postcopulatory traits is mediated by environmental conditions. To test how dietary resource availability affects sexual ornamentation, sperm quality and their interrelationship in three-spined sticklebacks (Gasterosteus aculeatus), full-sibling groups were raised under three conditions differing in food quantity and/or quality (i.e. carotenoid content): (i) high-quantity/high-quality, (ii) high-quantity/low-quality or (iii) low-quantity/low-quality. After 1 year of feeding, food-restricted males developed a more intense breeding coloration and faster sperm compared with their well-fed brothers, indicating that they allocated relatively more in pre- and postcopulatory traits. Moreover, they outcompeted their well-fed, carotenoid-supplemented brothers in sperm competition trials with equal numbers of competing sperm, suggesting that food-restricted males maximize their present reproductive success. This may result in reduced future reproductive opportunities as food-restricted males suffered from a higher mortality, had an overall reduced body size, and sperm number available for fertilization. In accordance with theory, a trade-off between the investment in pre- and postcopulatory traits was observed in food-restricted males, whereas well-fed males were able to allocate to both traits resulting in a significantly positive relationship.

Cain and Abel reloaded? Kin recognition and male–male aggression in three-spined sticklebacks Gasterosteus aculeatus L.

The influence of relatedness on male-male aggression was tested in three-spined sticklebacks Gasterosteus aculeatus. The intensity of aggression against brothers and non-kin males did not differ significantly, indicating that kin recognition plays at most a minor role in aggressive interactions between male G. aculeatus.

Functional variation of sperm morphology in sticklebacks

Some theoretical models of sperm competition make the assumption that in fish species with external fertilisation, sperm length relates positively to swimming speed at the expense of sperm longevity. Few studies have tested this assumption. We used the three-spined stickleback, Gasterosteus aculeatus L., to study functional sperm morphology. In this study, the relationship between males’ mean sperm length and fertilisation rate was investigated in vitro in a non-competitive situation. Fertilisation at different time points after sperm release was taken into account, and sperm morphology was quantified from scanning electron microscopy images. The time series of artificial fertilisations demonstrated that males which produced sperm with a longer tail fertilised faster, but their sperm had a shorter lifespan (or activity period). It was further suggested that males that produced sperm with a larger midpiece had greater fertilisation chances later on in the fertilisation process. Thus, in sticklebacks, there exists functional variation in sperm morphology, and sperm tail length is traded off against sperm longevity (or activity).