Strength of Sexual Selection and Sex Roles Vary between Social Groups in a Coral Reef Cardinalfish.

AbstractThe strength and direction of sexual selection can vary among populations. However, spatial variability is rarely explored at the level of the social group. Here we investigate sexual selection and sex roles in the paternally mouthbrooding, socially monogamous, and site-attached pajama cardinalfish, Sphaeramia nematoptera. Females were larger and more aggressive and had a longer dorsal fin filament, indicating reversed sex roles. At the scale of social groups, we show that the Bateman gradient and reproductive variance depend on the sex ratio and size of groups. In small and medium-sized groups with balanced or male-biased sex ratios, Bateman gradients were steeper for females, whereas gradients were equally steep for both sexes in large groups or when the sex ratio was female biased. For both sexes, reproductive variance increased with group size and with a higher male-to-female sex ratio. In S. nematoptera, mating opportunities outside the socially monogamous pair appear to impact sexual selection. We conclude that strength and direction of sexual selection can be masked by social dynamics in group-living species when considering only population and large-scale demographic processes.

Natal philopatry increases relatedness within groups of coral reef cardinalfish.

A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.

Extra-pair mating in a socially monogamous and paternal mouth-brooding cardinalfish.

Many vertebrates form monogamous pairs to mate and care for their offspring. However, genetic tools have increasingly shown that offspring often arise from matings outside of the monogamous pair bond. Social monogamy is relatively common in coral reef fishes, but there have been few studies that have confirmed monogamy or extra-pair reproduction, either for males or for females. Here, long-term observations and genetic tools were applied to examine the parentage of embryos in a paternally mouth-brooding cardinalfish, Sphaeramia nematoptera. Paternal care in fishes, such as mouth-brooding, is thought to be associated with a high degree of confidence in paternity. Two years of observations confirmed that S. nematoptera form long-term pair bonds within larger groups. However, genetic parentage revealed extra-pair mating by both sexes. Of 105 broods analysed from 64 males, 30.1% were mothered by a female that was not the partner and 11.5% of broods included eggs from two females. Despite the high paternal investment associated with mouth-brooding, 7.6% of broods were fertilized by two males. Extra-pair matings appeared to be opportunistic encounters with individuals from outside the immediate group. We argue that while pair formation contributes to group cohesion, both males and females can maximize lifetime reproductive success by taking advantage of extra-pair mating opportunities.

Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish.

Colonial animals often form stable pair bonds, returning to the same site to breed with the same partner every year. Familiarity with both partner and breeding site has the potential to enhance an individual's reproductive success. However, it is often unknown whether the mating system arises because of site fidelity, mate fidelity or both. Here, observational and experimental studies are used to identify causal links between site fidelity and pair formation in a group-living coral reef cardinalfish, Sphaeramia nematoptera. A long-term field tagging study was undertaken to quantify site and mate attachment. This was followed by both mate removal and mate transplant experiments to test whether the prolonged association with home sites was primarily because of mate or site fidelity. Adult S. nematoptera exhibited a prolonged association with home sites and partners, with some pairs lasting more than 4 months at the same site. A Bayesian mixed effect model showed that individuals in pairs were more likely to remain site attached, regardless of sex and maturity. Following mate removal, 78% of S. nematoptera found a new partner within 2 weeks on the same site, supporting the hypothesis that individuals primarily exhibit site fidelity. This was confirmed by the partner translocation experiment, with only 1 of 24 fish following their translocated partner to a new site. In these cardinalfish, strong site attachment facilitates long-lasting pair bonds, as well as new pair formation when necessary, suggesting that site rather than mate fidelity is the major driver of the reproductive system.

Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures.

Equatorial populations of marine species are predicted to be most impacted by global warming because they could be adapted to a narrow range of temperatures in their local environment. We investigated the thermal range at which aerobic metabolic performance is optimum in equatorial populations of coral reef fish in northern Papua New Guinea. Four species of damselfishes and two species of cardinal fishes were held for 14 days at 29, 31, 33, and 34 °C, which incorporated their existing thermal range (29-31 °C) as well as projected increases in ocean surface temperatures of up to 3 °C by the end of this century. Resting and maximum oxygen consumption rates were measured for each species at each temperature and used to calculate the thermal reaction norm of aerobic scope. Our results indicate that one of the six species, Chromis atripectoralis, is already living above its thermal optimum of 29 °C. The other five species appeared to be living close to their thermal optima (ca. 31 °C). Aerobic scope was significantly reduced in all species, and approached zero for two species at 3 °C above current-day temperatures. One species was unable to survive even short-term exposure to 34 °C. Our results indicate that low-latitude reef fish populations are living close to their thermal optima and may be more sensitive to ocean warming than higher-latitude populations. Even relatively small temperature increases (2-3 °C) could result in population declines and potentially redistribution of equatorial species to higher latitudes if adaptation cannot keep pace.

Sniffing out the competition? Juvenile coral reef damselfishes use chemical cues to distinguish the presence of conspecific and heterospecific aggregations.

Aquatic animals commonly rely on chemical cues to provide information regarding their surroundings. They can respond either by being attracted to (potential mates, preferred habitats) or avoiding (predators, competitors) the source of the stimuli. Coral reef fishes use chemical cues to detect habitats, avoid predators and recognise conspecifics. However, the extent to which chemical cues are used to detect and respond to potential competitors, has received little attention. Here we test olfactory preferences for conspecifics and heterospecifics in newly settled juvenile coral reef fishes. Juveniles of 4 common coral-associated damselfish species: Dascyllus melanurus, Dascyllus reticulatus, Chrysiptera arnazae and Pomacentrus moluccensis, were subjected to olfactory choice tests. Three of the 4 species (excluding P. moluccensis) demonstrated preferences for waterborne conspecifics odours. All species exhibited an avoidance towards heterospecific odours; this aversion was consistently greatest towards P. moluccensis. A neutral response toward heterospecifics was only evident in two instances (1) between the two congeneric Dascyllus species, with D. melanurus toward D. reticulatus, and (2) with C. arnazae toward D. melanurus. While it is already known that the presence of conspecifics plays a vital role in settlement site selection, we show here that the presence of heterospecifics may also be key in determining the spatial distributions of juveniles across areas of coral reef.

Relationships between pair formation, site fidelity and sex in a coral reef cardinalfish.

Coral reef fishes are characterised by extreme site fidelity and are often socially monogamous, forming pair bonds within larger social groups. Despite this, the strong link between reproductive behaviour and site fidelity in such social species is poorly understood. We examine these relationships in the cardinalfish Ostorhinchus cyanosoma on the central Great Barrier Reef. We tagged and followed over 100 individuals for 5 weeks to investigate pair fidelity, and behavioural differences between pairs and singles and between sexes, and we experimentally tested the strength of site and mate fidelity. Tagged pairs were typically highly site attached, and lasted throughout the study period. Sex had very little effect on pairing behaviour or habitat use. Paired individuals showed three times higher site fidelity than single ones, with singles frequently relocating. There was a two-fold increase in the movement of individuals that had their partners experimentally removed. Paired individuals exhibited greater homing success, and homed regardless of whether their mate had been displaced with them or was left on the home site. These results suggest that individuals of this species form at least seasonally stable monogamous pair bonds within larger groups, and that pair formation is closely associated with site fidelity.

Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures.

The response of species to global warming depends on how different populations are affected by increasing temperature throughout the species' geographic range. Local adaptation to thermal gradients could cause populations in different parts of the range to respond differently. In aquatic systems, keeping pace with increased oxygen demand is the key parameter affecting species' response to higher temperatures. Therefore, respiratory performance is expected to vary between populations at different latitudes because they experience different thermal environments. We tested for geographical variation in respiratory performance of tropical marine fishes by comparing thermal effects on resting and maximum rates of oxygen uptake for six species of coral reef fish at two locations on the Great Barrier Reef (GBR), Australia. The two locations, Heron Island and Lizard Island, are separated by approximately 1200 km along a latitudinal gradient. We found strong counter-gradient variation in aerobic scope between locations in four species from two families (Pomacentridae and Apogonidae). High-latitude populations (Heron Island, southern GBR) performed significantly better than low-latitude populations (Lizard Island, northern GBR) at temperatures up to 5°C above average summer surface-water temperature. The other two species showed no difference in aerobic scope between locations. Latitudinal variation in aerobic scope was primarily driven by up to 80% higher maximum rates of oxygen uptake in the higher latitude populations. Our findings suggest that compensatory mechanisms in high-latitude populations enhance their performance at extreme temperatures, and consequently, that high-latitude populations of reef fishes will be less impacted by ocean warming than will low-latitude populations.