Genetic life history effects on juvenile survival in bluegill

Foraging behaviour under the risk of predation has important consequences on an individual's survivorship and fitness. In bluegill (Lepomis macrochirus), we have recently shown that offspring sired by males of alternative life histories differ in their foraging behaviour. Specifically, offspring sired by 'cuckolder' males take fewer risks during foraging than do offspring sired by 'parental' males. This behavioural difference can have important consequences on the fitness of the two life histories and thus the underlying evolutionary mechanism. Here, we examine the consequences of this behavioural variation on growth rate, condition and survivorship during early development of juveniles. We used split in vitro fertilization to generate maternal half-sibs that differed in sire life history. The resulting 18 455 larvae from 50 families were released into a microcosm with safe and risky foraging areas for approximately 2 months. A total of 262 juveniles (1.4%) survived of which parentage was unambiguously determined using microsatellite genetic markers for 254 (97%). Although we found significant dam effects, there was no difference in apparent growth rate or condition of juveniles sired by males of the two life histories. Of the 25 paired half-sib families, 15 had higher survivorship when sired by a cuckolder male, seven had higher survivorship when sired by a parental male and three had no surviving offspring from either sire. Thus, although growth was similar between the two offspring types, survivorship was not. Combining the differential survivorship estimate with paternity data from natural nests and the frequency of males adopting each life history, we calculated that the cuckolder life history has 1.87 times higher fitness than the parental life history. As such, the life histories likely are not governed by a genetic polymorphism.     

In Vitro Fertilization Reveals Offspring Recognition via Self-Referencing in a Fish with Paternal Care and Cuckoldry

Male bluegill sunfish (Lepomis macrochirus) exhibit alternative life histories: some males (parentals) delay maturation for up to 7 yr, then build nests, court females, and care for the eggs and fry, whereas other males (cuckolders) mature precociously, attempt to steal fertilizations from parentals, and provide no parental care. Parental males could avoid misdirecting their nepotism (i.e. caring for unrelated young) by abandoning entire broods if they were sired mainly by cuckolders or by discriminating between offspring and non‐kin fry within broods for which they care. We tested for kin discrimination by obtaining sperm from parental and cuckolder males and eggs from several females, and using them to conceive fry in vitro. In ‘blind’ laboratory tests, parental males (but not cuckolder males) distinguished between sources of dripping water that had been conditioned by their own offspring vs. unrelated fry. Parental males that were in the best physical condition were especially choosy. Because the only referents available to our experimental subjects were chemical cues emanating from their own body, our results imply that parental males can use self‐referent phenotype matching for kin recognition. This mechanism enables males to make the adaptive, nepotistic adjustments in paternal care that have been documented in previous studies.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Promiscuity drives self-referent kin recognition

Kin selection theory has been one of the most significant advances in our understanding of social behavior . However, the discovery of widespread promiscuity has challenged the evolutionary importance of kin selection because it reduces the benefit associated with helping nestmates . This challenge would be resolved if promiscuous species evolved a self-referent kin-recognition mechanism that enables individuals to differentiate kin and nonkin . Here, we take advantage of an asymmetry in the level of promiscuity among males of alternative life histories in the bluegill sunfish (Lepomis macrochirus). We show that, as a consequence of this asymmetry, offspring of "parental" males have a high level of relatedness to nestmates, whereas offspring of "cuckolder" males have a low level of relatedness to nestmates. We find that offspring of parentals do not use a direct recognition mechanism to discriminate among nestmates, whereas offspring of cuckolders use kin recognition by self-referent phenotype matching to differentiate between kin and nonkin. Furthermore, we estimate that the cost of utilizing such self-referent kin recognition is equivalent to a relatedness (R) of at least 0.06. These results provide compelling evidence for adaptive use of kin recognition by self-referent phenotype matching and confirm the importance of kinship in social behavior.     

Paternity and egg cannibalism in the ringlegged earwig Euborellia annulipes (Dermaptera: Anisolabididae)

Cannibalism is a common occurrence in nature, and many cannibals prey on relatively small and defenseless life stages, such as eggs or young juveniles. Such behavior provides many benefits to the cannibal, but cannibalistic individuals also face risks, including the cost of decreasing their inclusive fitness by eating close relatives such as siblings or offspring. This risk can be mitigated if cannibals can recognize and avoid preying on kin. Here, we tested whether male ringlegged earwigs Euborellia annulipes avoid cannibalizing eggs that they had sired. In this species, females care for their own eggs, but males provide no care and frequently prey upon eggs. We found that when presented with an unguarded clutch of eggs, male earwigs nearly always cannibalized some eggs, but that the proportion of eggs eaten was smaller if the male had sired the clutch. This suggests that males can distinguish between their own offspring and unrelated offspring and that they avoid harming their kin.     

Extra‐group mating increases inbreeding risk in a cooperatively breeding bird

In many cooperatively breeding species, females mate extra‐group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra‐group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra‐group mating decisions and, moreover, extra‐group mating females were significantly more related to their extra‐group sires than their social mates. Instead, dominant females were substantially more likely to mate extra‐group when paired to a dominant male of low heterozygosity, and their extra‐group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra‐group males of closer relatedness, but higher heterozygosity resulted in extra‐group‐sired offspring that were no more heterozygous than their within‐group‐sired half‐siblings. Our findings are consistent with a role for male–male competition in driving extra‐group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra‐group by exposing them to a risk of inbreeding.     

Kin recognition affects plant communication and defence

The ability of many animals to recognize kin has allowed them to evolve diverse cooperative behaviours; such ability is less well studied for plants. Many plants, including Artemisia tridentata, have been found to respond to volatile cues emitted by experimentally wounded neighbours to increase levels of resistance to herbivory. We report that this communication was more effective among A. tridentata plants that were more closely related based on microsatellite markers. Plants in the field that received cues from experimentally clipped close relatives experienced less leaf herbivory over the growing season than those that received cues from clipped neighbours that were more distantly related. These results indicate that plants can respond differently to cues from kin, making it less likely that emitters will aid strangers and making it more likely that receivers will respond to cues from relatives. More effective defence adds to a growing list of favourable consequences of kin recognition for plants.     

Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata

Although kin associations between fish can develop in the laboratory, the importance of kin structure in natural social groups remains uncertain. Guppies ( Poecilia reticulata ) possess many behavioural and life-history traits that promote kin structure, and so constitute ideal candidates for testing its general significance amongst fish. We collected 25 adult only shoals from ∼150 m stretches along two Trinidadian rivers. The 272 sampled fish were genotyped from a pool of seven hypervariable microsatellite loci. Although mark-recapture experiments have previously detected male-biased dispersal, which is predicted from the guppy mating system and which may have important implications for population differentiation, we found no sex-biases in dispersal between shoals. Because sex-biased dispersal was not evident, males and females were pooled in analyses of kin structure. Relatedness levels within each shoal did not differ significantly from zero, indicating that kin selection does not contribute to gross structure. Instead, our data is more consistent with the hypothesis that individual-level selection underlies shoal composition dynamics. These dynamics have important implications for the evolution of cooperative behaviour in guppies.     

Mosquito oviposition and larvae development in response to kairomones originated by different fish

Predator‐released kairomones indicating the presence of predatory fish are known to alter the behaviour and life‐history traits of several aquatic herbivores. Culex mosquitoes (Diptera: Culicidae) respond to such cues by altering oviposition habitat selection and larval development time. These responses differ among fish species indicating composition differences among fish‐released cues, but the recognition pattern is not clear. This study tested the dependence of fish recognition to co‐evolution and the level of threat to larvae. We compared Culex responses to three fish, the invasive larvivorous Gambusia affinis (Cyprinodontiformes: Poeciliidae), the native larvivorous Aphanius mento (Cyprinodontiformes: Cyprinodontidae) and the native algivorous Garra rufa (Cypriniformes: Cyprinidae). The effects of cues released by the three fish on Culex oviposition and life‐history shifts were compared in field mesocosms and lab tests. Our results showed that ovipositing females were significantly repelled only by cues originated from G. affinis, while developing larvae response was a more general one. Our results support the idea that fish‐released kairomones differ in composition or quantities among different species.     

Influence of Kinship and MHC Class II Genotype on Visual Traits in Zebrafish Larvae (Danio rerio)

Kin recognition can drive kin selection and the evolution of social behaviour. In zebrafish (Danio rerio, Hamilton 1822), kin recognition is based on olfactory and visual imprinting processes. If larvae are exposed to visual and chemical cues of kin at day 5 and 6 post fertilization they will recognize kin throughout life, while exposure to non-kin fails to trigger any recognition. Chemical imprinting signals are transcribed by polymorphic genes of the major histocompatibility complex (MHC) code; however, the underlying mechanism for visual imprinting remains unclear. Here we provide evidence for the existence of family-specific differences in morphometry and pigmentation pattern of six day old zebrafish larvae. While rump, tail and body pigmentation were dependent on relatedness, iris pigmentation and morphometry were also influenced by MHC class II genotype. Our study revealed that the MHC not only influences the chemical signature of individuals, but also their visual appearance.     

Cannibalizing Harmonia axyridis (Coleoptera: Coccinellidae) larvae use endogenous cues to avoid eating relatives

Cannibalism is widespread among many different organisms, and can have both negative and positive fitness consequences. Avoiding eating relatives can minimize negative fitness consequences of cannibalism. Such avoidance requires kin discrimination, but evidence for this ability among cannibals is limited with little data that address the cues used in such discrimination. We examined whether larvae of the ladybird beetle Harmonia axyridis avoid eating their relatives. We further manipulated environmental factors to create individuals that had similar or dissimilar rearing environments to begin to test for endogenous versus exogenous recognition cues. In our experiments, third-instar larvae were much less likely to cannibalize if they were interacting with a relative. Larvae that did cannibalize kin required more encounters, and significantly delayed cannibalism, compared to larvae cannibalizing unrelated individuals. Acquired cues were less important. Even though the different rearing environment resulted in significantly different phenotypic effects, similarity or dissimilarity of rearing environment had no effect on cannibalism, and there was no interaction between environments and relatedness in cannibalism. We suggest that H. axyridis has a well-developed kin discrimination system, and that kin recognition in this ladybird beetle is based on endogenous rather than exogenous cues. We also argue that these cues reflect either direct or indirect genetic effects on larval phenotypes.     

Paternal Genetic Effects on Foraging Decision-Making Under the Risk of Predation

Foraging behavior under the risk of predation has interested biologists for decades. Here, we examine paternal genetic effects on foraging decisions of bluegill (Lepomis macrochirus) larvae sired by males adopting alternative life histories. We use split in vitro fertilization to generate maternal half‐siblings sired by either a ‘parental’ male or a ‘cuckolder’ male. Immediately, upon the switch to exogenous feeding, we fed the larvae ad libitum for 2 d. We then starved the larvae for between 12 and 17 h, following which we subjected them to a dichotomous choice foraging trial, where one side of a test tank posed a risky foraging habitat and the other posed a safe foraging habitat. Equal amounts of food were simultaneously introduced to both sides of the tank and the proportion of individuals on either side was recorded. There were significantly fewer cuckolder offspring foraging on the risky side of the tank when compared with their parental half‐siblings indicating that cuckolder offspring took fewer risks than parental offspring. These results demonstrate a paternal genetic effect (sire life history) on foraging behavior. We ruled out energetic state as a possible explanation for this difference because the half‐siblings did not differ in body length or mass. Instead, previous research suggests that cuckolder offspring have higher conversion efficiency (efficiency of converting food into soma) than parental offspring and therefore the differences in foraging behavior observed here may, in part, be attributed to genetic differences in conversion efficiency.     

Orientation of larval and juvenile horseshoe crabs Limulus polyphemus to visual cues:Effects of chemical odors

Adult horseshoe crabs Limulus polyphemus have long served as models for the study of vision in marine arthropods. Yet,little is known about the ability of early life history stages to detect and respond to visual cues.We examined the visually directed movements of larvae and first stage juveniles to horizons containing dark visual targets of different sizes.The study tested the hypotheses that (1) larval and juvenile crabs can detect and respond to visual targets and (2) the direction of orientation varies ...     

Investigating the Effect of Familiarity on Kin Recognition of Three‐Spined Stickleback (Gasterosteus aculeatus)

The ability to discriminate between related and unrelated individuals has been demonstrated in many species. The mechanisms behind this ability might be manifold and depend on the ecological context in which the species lives. In brood‐caring species, both familiarity and phenotype matching are known to be used in kin recognition. However, results of studies disentangling these two phenomena have proved contradictory. We aimed to broaden our knowledge about the mechanisms of kin recognition using shoaling preferences of three‐spined stickleback (Gasterosteus aculeatus) as a model behavior. In our first experiment, focal fish had the choice to shoal either with kin or unfamiliar non‐kin. In half of the trials, kin groups were composed of familiar individuals, while they were unfamiliar in the other half. Focal fish significantly preferred kin as shoaling partner, a result which was not reinforced by familiarity. In our second experiment, focal fish were given the choice between a shoal of familiar kin and a shoal of unfamiliar kin. Here, focal fish did not show any significant preference. These results indicate that familiarity does not impact stickleback's ability to recognize kin. Furthermore, they show that familiarity does not overrule recognition based on phenotype matching or innate recognition, underlining the importance of these mechanisms. Finally, our results lead to the assumption that individual recognition might play a minor role also in non‐kin‐based preferences for familiars.     

Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura

Environments vary stochastically, and animals need to behave in ways that best fit the conditions in which they find themselves. The social environment is particularly variable, and responding appropriately to it can be vital for an animal’s success. However, cues of social environment are not always reliable, and animals may need to balance accuracy against the risk of failing to respond if local conditions or interfering signals prevent them detecting a cue. Recent work has shown that many male Drosophila fruit flies respond to the presence of rival males, and that these responses increase their success in acquiring mates and fathering offspring. In Drosophila melanogaster males detect rivals using auditory, tactile and olfactory cues. However, males fail to respond to rivals if any two of these senses are not functioning: a single cue is not enough to produce a response. Here we examined cue use in the detection of rival males in a distantly related Drosophila species, D. pseudoobscura, where auditory, olfactory, tactile and visual cues were manipulated to assess the importance of each sensory cue singly and in combination. In contrast to D. melanogaster, male D. pseudoobscura require intact olfactory and tactile cues to respond to rivals. Visual cues were not important for detecting rival D. pseudoobscura, while results on auditory cues appeared puzzling. This difference in cue use in two species in the same genus suggests that cue use is evolutionarily labile, and may evolve in response to ecological or life history differences between species.     

The kin selection hypothesis in a lekking mole cricket: assessing nested patterns of relatedness

Loosely defined, a lek is a male mating aggregation visited by females primarily for the purpose of fertilization. No consensus has been forged that successfully explains how and why leks have evolved across the full breadth of lekking taxa. The two major conceptual explanations (cooperation and competition) are both intricately intertwined in any given system and exhibit varying levels of plasticity based on an organism's environment and life history. The kin selection hypothesis suggests that if females prefer larger leks (as is often the case), unattractive males may aggregate with their attractive relatives in order to boost the latter's reproductive success, while effectively sacrificing any opportunities of their own. Here we develop microsatellite markers to genetically evaluate the kin selection hypothesis by measuring relatedness and precise spatial locations of males in a population of the lekking prairie mole cricket (Gryllotalpa major Saussure). Results indicate that neighbouring males are often highly related, suggesting that kin selection may play some role in this system. However, because leks are comprised of multiple kin groups, if kin selection is operating it is likely doing so at a smaller scale than predicted by the kin selection hypothesis of lek formation. The high levels of subgroup relatedness within this species likely occurs as a passive process due to male viscosity, but the functional implications of this interesting genetic organization remain unknown.     

Natural Populations of Shipworm Larvae Are Attracted to Wood by Waterborne Chemical Cues

The life cycle of many sessile marine invertebrates includes a dispersive planktonic larval stage whose ability to find a suitable habitat in which to settle and transform into benthic adults is crucial to maximize fitness. To facilitate this process, invertebrate larvae commonly respond to habitat-related chemical cues to guide the search for an appropriate environment. Furthermore, small-scale hydrodynamic conditions affect dispersal of chemical cues, as well as swimming behavior of invertebrate larvae and encounter with potential habitats. Shipworms within the family Teredinidae are dependent on terrestrially derived wood in order to complete their life cycle, but very little is known about the cues and processes that promote settlement. We investigated the potential for remote detection of settling substrate via waterborne chemical cues in teredinid larvae through a combination of empirical field and laboratory flume experiments. Natural populations of teredinid larvae were significantly more abundant close to wooden structures enclosed in plankton net compared to empty control nets, clearly showing that shipworm larvae can sense and respond to chemical cues associated with suitable settling substrate in the field. However, the flume experiments, using ecologically relevant flow velocities, showed that the boundary layer around experimental wooden panels was thin and that the mean flow velocity exceeded larval swimming velocity approximately 5 mm (≈ 25 larval body lengths) from the panel surface. Therefore, we conclude that the scope for remote detection of waterborne cues is limited and that the likely explanation for the higher abundance of shipworm larvae associated with the wooden panels in the field is a response to a cue during or after attachment on, or very near, the substrate. Waterborne cues probably guide the larva in its decision to remain attached and settle, or to detach and continue swimming and drifting until the next encounter with a solid substrate.     

Biofilm history and oxygen availability interact to affect habitat selection in a marine invertebrate

In marine systems, oxygen availability varies at small temporal and spatial scales, such that current oxygen levels may not reflect conditions of the past. Different studies have shown that marine invertebrate larvae can select settlement sites based on local oxygen levels and oxygenation history of the biofilm, but no study has examined the interaction of both. The influence of normoxic and hypoxic water and oxygenation history of biofilms on pre-settlement behavior and settlement of the bryozoan Bugula neritina was tested. Larvae used cues in a hierarchical way: the oxygen levels in the water prime larvae to respond, the response to different biofilms is contingent on oxygen levels in the water. When oxygen levels varied throughout biofilm formation, larvae responded differently depending on the history of the biofilm. It appears that B. neritina larvae integrate cues about current and historical oxygen levels to select the appropriate microhabitat and maximize their fitness.     

Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates

Where animals avoid inbreeding, different mechanisms of kin discrimination can leave different 'signatures' in the patterns of observed mate relationship. For example, consider a species with no paternal care. If a female avoids mating with familiar individuals, one would expect a deficit of offspring whose parents are maternal half-siblings, but paternal half-siblings would be unfamiliar with each other and thus have offspring at the frequency expected by chance. If spatial cues are used to avoid inbreeding, a female would be expected to produce few offspring with males (even unrelated males) living near her birth site. We searched for these and other signatures with data from a long-term study of banner-tailed kangaroo rats, Dipodomys spectabilis, in Arizona, USA, using a combination of intensive censusing, mapping of available dens, microsatellite-based parentage determination, and a randomization routine that determines the numbers of offspring expected if females in the population mate indiscriminately among the males available to them. The data are consistent with the hypothesis that kangaroo rats discriminate kin by familiarity developed via association early in life, rather than by using spatial cues or self-referential phenotype matching. Our approach should be widely applicable as a means of assessing the degree to which kin discrimination exists (in contexts like nepotism as well as inbreeding avoidance) and in inferring what cues animals use to assess categories of relationship.     

Larval Ischnura verticalis (Odonata: Coenagrionidae) Respond to Visual Cues of Predator Presence

Larvae of some species of damselflies respond to chemical cues of fish predators but, while larvae of many species are thought to detect prey through vision, there is little evidence that larvae respond to visual cues of predator presence. This laboratory study indicated larval Ischnura verticalis behaviours are affected by visual cues and, to a much lesser extent, chemical cues of fish; there was no significant interaction between the effects of visual and chemical cues. Responses to chemical cues of fish did not depend on whether fish were fed I. verticalis larvae versus commercial fish food. Larvae were more active in the spring than the fall when they were likely in diapause. Results suggest larvae can use vision to detect large, active predators but can also detect predators through olfaction when visual cues are unreliable.