Inbreeding Depression and Inbreeding Avoidance in a Natural Population of Guppies (Poecilia reticulata)

Maintenance of genetic variation in the face of strong natural selection is a long‐standing problem in evolutionary biology. One of the most extreme examples of within‐population variation is the polymorphic, genetically determined color pattern of male Trinidad guppies (Poecilia reticulata). Female mating preference for rare or novel patterns has been implicated as a factor in maintaining this variation. The origin of this preference is not understood, although inbreeding avoidance has been proposed as a mechanism. Inbreeding avoidance is advantageous when populations exhibit inbreeding depression and the opportunity for mating between relatives exists. To determine whether these conditions are met in a natural guppy population, we assessed mating and reproductive patterns using polymorphic molecular markers. Females produced more offspring with less‐related males than with more‐related ones. In addition, females were more likely to have mated with less‐related males, but this trend was only marginally significant. Male heterozygosity was positively correlated with mating success and with the number of offspring sired, consistent with strong inbreeding depression for adult male fitness. These results provide substantial insight into mating patterns of a wild guppy population: strong inbreeding depression occurs, and individuals tend to avoid mating with relatives.     

Interactions Among Female Guppies (Poecilia reticulata) Affect Growth and Reproduction

Competition among females over resources may have consequences for their resource budgets and thereby the resource allocation between growth and reproduction. In addition, the consequences of female–female interactions may differ for dominant and subordinate individuals, with the dominant ones being at an advantage. In this study, we investigated the consequences of female–female competition in guppies by manipulating the competitive environment of females. We found that large guppy females dominated smaller females and that interactions between females likely are costly because females exposed to competition grew less. These females compensated by growing at a higher rate when no longer subjected to competition. The higher growth rate might in turn be the cause of the reduced reproductive effort in the more competitive treatments. Furthermore, interactions were more costly for females when they were in the subordinate role than in the dominant role, because the reduction in growth and reproductive effort was highest in females exposed to larger competitors. Whether there was a differential allocation of resources into growth and reproduction depending on dominance status needs further investigation. However, in general, smaller females had a higher growth rate than larger females, independent of competitive level. We also found a negative relationship between reproduction and growth in all treatments, indicating a cost of reproduction.     

Observational Learning and Predator Inspection in Guppies (Poecilia reticulata)

Prior work has demonstrated that, following a predator inspection visit of their own, guppies prefer to associate with individuals who inspected a predator most closely. Based on this work, as well as studies of social learning in the context of mate choice, we predicted that male guppies that observed but did not participate in an inspection trial would subsequently choose to associate with the closer of two inspectors. Our experimental protocol consisted of three treatments: a control test in which an observer watched two fish consecutively, only one of which was exposed to a predator, a sequential test in which an observer watched two fish consecutively, both of which were exposed to the predator, and a social test in which an observer watched two fish inspect simultaneously. We found no preferences by the observer for either of the fish in any of the trials. Our results suggest that direct interaction is a critical component to the development of preferences in male guppies. We discuss our findings in light of game theoretical treatments of cooperation.     

Endocrine Disrupting Compounds Alter Risk‐Taking Behavior in Guppies (Poecilia reticulata)

Endocrine disrupting compounds (EDCs) enter aquatic habitats from a variety of anthropogenic sources and can mimic, block, or modulate the synthesis of natural hormones. EDCs affect both reproductive and non‐reproductive behaviors because hormones mediate responses associated with aggression and fear. We examined the effects of two EDCs on risk‐taking behaviors in guppies (Poecilia reticulata). We quantified risk‐taking in terms of propensity to forage in a risky location and tendency to join groups in the presence of a predator. We found that male and female guppies responded oppositely to environmentally relevant concentrations of an estrogenic EDC, 17α‐ethinylestradiol (EE2), or an androgenic EDC, 17β‐trenbolone (TB). Males decreased risk‐taking with increasing EE2 concentration (as predicted), but females increased risk‐taking (contrary to prediction). In contrast, females increased risk‐taking with increasing TB concentrations (as predicted), but males decreased risk‐taking (contrary to prediction). These results did not match our expectation that EE2 would reduce risk‐taking and TB would increase risk‐taking in both sexes. We suspect EE2 and TB produced these counterintuitive effects by downregulating their corresponding hormone receptors and thus reducing levels of circulating endogenous hormones in females and males, respectively. These results show that EDCs can alter fish behavior and potentially reduce fitness in unexpected ways.     

The Effect of Social Environment on Male–Male Competition in Guppies (Poecilia reticulata)

We examined male–male competition in guppies (Poecilia reticulata) to test for evidence of hierarchy formation and any subsequent effects on male mating success by comparing the interactions of pairs of males that were siblings and life‐long tank mates with those of unrelated pairs that had never met. These pairs of males were first observed in the absence of a female; then a female was added to gauge the effects of the initial male–male interactions on male sexual behaviour. The unfamiliar/unrelated pairs engaged in significantly more aggressive interactions such as physical contacts, nipping and chasing than the familiar/related pairs. Based on several previous studies, we suggest that familiarity played a greater role than relatedness in the differences in behaviour that we observed. Our results suggest that, in some circumstances, more aggressive males may have more mating opportunities than less aggressive males. Our results also indicate that males adjust their aggressive and courtship behaviours to the perceived intensity of competition for mates, based on the number of mature males in their rearing tanks. We suggest that male–male competition for mating opportunities may play a more important role in the guppy mating system than previously thought.     

Population Differences in the Schooling Behaviour of Newborn Guppies,Poecilia reticulata

Population differences in the schooling behaviour of adult guppies (Poecilia reticulata) from Trinidad have previously been well documented. This paper demonstrates that variation in schooling behaviour is also present in newborn fish. Guppies from the Aripo River of Trinidad display well-developed schooling behaviour from birth. In addition to forming cohesive and polarized groups, these newborn fish also exhibit predator inspection behaviour. Newborn guppies from the Paria River perform inspections but, unlike the Aripo fish, are poor schoolers. Population variation in behaviour at birth does not necessarily reflect the pattern observed in the adult fish. As adults, guppies from the Upper section of the Aripo River have a much lower schooling tendency and are less wary during inspection than the downstream Lower Aripo guppies. At birth, however, the schooling behaviour and inspection behaviour in the two populations is identical. These results suggest that different selective pressures operate on adult and newborn guppies in Trinidad.     

The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history. Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness. Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.     

Female preference for blue in Japan blue guppies (Poecilia reticulata)

Guppies (Poecilia reticulata) are widely used as a model species in mate choice studies. Although native to South America, guppies have been introduced to natural water bodies in disparate regions of the globe. Here, for the first time, we examine guppies from one such introduced population in Japan where males have evolved a predominantly blue color pattern. Previous studies of wild-type guppies have shown blue to play a relatively minor role in the mate choice decisions of females compared to other traits, such as orange, and the importance of blue is not universally supported by all studies. The Japanese population therefore presents an ideal opportunity to re-examine the potential significance of blue as a mate choice cue in guppies. Mate choice experiments, in which female Japan blue guppies were given a choice between pairs of males that differed in their area of blue coloration but were matched for other traits, revealed that females prefer males with proportionately larger amounts of blue in their color patterns. We discuss possible factors, including sexual and ecological selection, which may have led to the evolution of unusually large areas of blue at the expense of other colors in Japan blue guppies. However, further studies are needed to distinguish between these scenarios.     

Interpopulation Differences in Shoaling Behaviour in Guppies (Poecilia reticulata): Roles of Social Environment and Population Origin

In Trinidad, guppies (Poecilia reticulata) in high‐predation localities show more cohesive shoaling behaviour than those living with less dangerous predators in low‐predation sites. We evaluated the relative contributions of population origin (i.e. genetic and/or maternal effects) and social environment on the expression of shoaling by assessing the behaviour of juveniles reared in a range of social conditions. Focal individuals, offspring of guppies from populations from high‐ or low‐predation localities, were reared in a multifactorial experiment; we created four different social conditions by manipulating the source and demography of the conspecific residents with whom focal individuals interacted. We found that high‐predation fish displayed a stronger propensity to shoal than low‐predation ones. Our results also suggest a role for interactions between the source of the focal individuals, the demography of the group in which they were reared and the origin of the guppies with whom they were reared. Depending on their origin (high‐ vs. low‐ predation) and rearing density, our focal fish were more likely to shoal if they were reared with high‐predation residents. Learning from high‐predation residents, aggressive interactions with low‐predation residents and/or phenotype matching could have played a role in driving this effect of social environment. This effect of the phenotype of conspecifics on shoaling development would enhance heritable differences in shoaling propensity such that both could contribute to the well‐documented difference in shoaling behaviour of high‐ and low‐predation guppies in natural populations.     

Female preferences based on olfactory cues in the guppy (Poecilia reticulata)

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Gametic isolation in guppies (Poecilia reticulata)

Post-mating reproductive isolating mechanisms may be among the earliest reproductive barriers to emerge among incipient species. Trinidadian guppy, Poecilia reticulata, populations in the Caroni and Oropouche drainages in Northern Trinidad exhibit marked genetic divergence and provide an ideal system in which to search for these barriers. We inseminated virgin females with equal amounts of sperm from two males, a 'native' male from the female's own population and a 'foreign' male from the other drainage. Artificial insemination ensured that mating order and mate choice did not affect the outcome. Paternities were assigned to the resulting broods using microsatellite markers. As predicted, sperm from native males had precedence over foreign sperm. Moreover, this effect was symmetrical for both drainages. In contrast, we detected no native sperm precedence in controls, in which females received sperm from the same and another population within the same drainage. Our results show that gametic isolation can arise between geographically proximate, though genetically divergent, populations of a single species and highlight the potential role of this process in speciation.     

Male Mating History Influences Female Mate Choice in the Trinidadian Guppy (Poecilia reticulata)

Based on the phenotype‐linked fertility hypothesis, sexual selection should favour females that can accurately assess the recent mating history of available sexual partners and preferentially avoid mating with recently‐mated males [who may be sperm depleted (SD)] so as to minimize the risk of their eggs not being fertilized. This hypothesis has received to date only limited attention and empirical support. Therefore, in the current study, we investigated experimentally whether females of a vertebrate species, the Trinidadian guppy (Poecilia reticulata), are able to assess the recent mating history of males, and thus potentially their functional fertility, and choose to avoid mating with males that appear to have recently mated and who may be sperm limited. Individual virgin females were first given a dichotomous choice between a male that had not been recently observed to interact sexually with another female (i.e. not sperm‐depleted) and another male that had been observed to interact sexually with a female (i.e. potentially sperm‐depleted) as sexual partners. Paired males were matched for body length and coloration. Immediately following this test, the focal females were subjected to a free‐swimming mate‐choice test using the same paired stimulus males. As predicted, on average, female guppies avoided the apparently recently‐mated (and potentially sperm‐depleted) male and exhibited a significant preference for the other male not recently observed mating (and thus not likely sperm limited) during both tests. We do not yet fully understand the underlying mechanisms of this preference. Therefore, further research on the particular cues that females use to assess the recent mating history and fertility status of males is required.     

Molecular Phylogeny and Genetic Divergence of the Introduced Populations of Japanese Guppies, Poecilia reticulata

A phylogenetic tree of guppies from seven introduced Japanese populations was constructed using a mitochondrial gene, and the relationship between these Japanese populations and indigenous South American populations was examined. Phylogenetic trees constructed by maximum parsimony and neighbor joining methods indicated four major groups: Group A: Trinidadian populations; Group B: the northernmost Okinawa populations; Group C: the northern Okinawa populations; Group D: Shimoda populations and the remainder of Trinidadian, Venezuelan, and southern Okinawa populations. Considerable genetic differences were observed among the haplotypes within each Okinawa population similar to that found among haplotypes of different native populations, but not within the Shimoda population, because each Okinawa population included haplotypes belonging to different groups. Genetic differences between Groups B, C, and D might reflect those of the introduced lineages; however, these differences might not result from the divergence after introduction events. These results suggested that multiple introductions of different breeding lineages might cause considerable divergence within and between Okinawa populations.     

Female mate preference explains countergradient variation in the sexual coloration of guppies (Poecilia reticulata)

We tested the hypothesis that mate choice is responsible for countergradient variation in the sexual coloration of Trinidadian guppies (Poecilia reticulata). The nature of the countergradient pattern is that geographical variation in the carotenoid content of the orange spots of males is counterbalanced by genetic variation in drosopterin production, resulting in a relatively uniform pigment ratio. A female hue preference could produce this pattern, because hue is the axis of colour variation most directly affected by the pigment ratio. To test this hypothesis, we crossed two populations differing in drosopterin production and produced an F(2) generation with variable drosopterin levels. When the carotenoid content of the orange spots was held constant, female guppies preferred males with intermediate drosopterin levels. This shows that females do not simply prefer males with greater orange spot pigment content; instead, the ratio of the pigments also affects male attractiveness. To our knowledge, this is the first direct evidence for a hypothesized agent of countergradient sexual selection.     

Female mate copying in the guppy {Poecilia reticulata): age-dependent effects

Virtually all studies of mate choice to date have assumed thatfemales choose mates independent of one another. Social cues,however, such as the mate choice of conspecifics, may also playan important role in such decisions. Previous work has shownthat female guppies of similar age copy each other's choiceof mates. Here we examine the effect of relative age on matechoice copying in the guppy, Poecilia reticulata, and examinewhether younger individuals are more likely to copy the matechoice of older conspecifics than vice versa. Results indicatethat younger females copy the mate choice of older females,but older individuals do not appear to be influenced by themate choice of younger individuals.     

Discriminating between Hungry and Satiated Predators: The Response of Guppies (Poecilia reticulata) from High and Low Predation Sites1

Fixed anti-predator activities are costly because they limit the ability of the prey to take advantage of short term temporal patchiness in predation pressure. The ability to discriminate between hungry and satiated predators and a flexible response to the differential threat can help to lower the costs of anti-predator behavior. In this study Trinidadian guppies (Poecilia reticulata) were found to distinguish between hungry and satiated predators. In Trinidad, populations of guppies experience different levels of predation from piscivorous fish. Individuals taken from populations with chronically high predation pressure responded stronger to the hungry predator than those from low predation sites.     

Orange Spots as a Visual Cue for Female Mate Choice in the Guppy (Poecilia reticulata)

Previous studies have suggested that orange pigment in the color patterns of male guppies is a cue for female choice. This paper describes a manipulative experiment designed to test this hypothesis. The color patterns perceived by females were manipulated by varying the color of light used to illuminate the experimental aquaria. Orange light dramatically reduces the conspicuousness of orange spots to human observers, and probably also to female guppies. As in previous experiments, female guppies discriminated among males based on differences in the extent of orange pigment, under white, blue, and green light conditions. Under orange light, however, females no longer appeared to discriminate on the basis of orange spots. These results support the hypothesis that orange spots, rather than other correlated characteristics, are a basis for female choice under normal lighting conditions.     

Aerial Jumping in the Trinidadian Guppy (Poecilia reticulata)

Many fishes are able to jump out of the water and launch themselves into the air. Such behavior has been connected with prey capture, migration and predator avoidance. We found that jumping behavior of the guppy Poecilia reticulata is not associated with any of the above. The fish jump spontaneously, without being triggered by overt sensory cues, is not migratory and does not attempt to capture aerial food items. Here, we use high speed video imaging to analyze the kinematics of the jumping behavior P. reticulata. Fish jump from a still position by slowly backing up while using its pectoral fins, followed by strong body trusts which lead to launching into the air several body lengths. The liftoff phase of the jump is fast and fish will continue with whole body thrusts and tail beats, even when out of the water. This behavior occurs when fish are in a group or in isolation. Geography has had substantial effects on guppy evolution, with waterfalls reducing gene flow and constraining dispersal. We suggest that jumping has evolved in guppies as a behavioral phenotype for dispersal.     

Female guppies Poecilia reticulata prefer males that can learn fast

The role of learning ability as a potentially desirable male trait in sexual selection was investigated in the guppy Poecilia reticulata . Mate preference tests and the rate at which a male learnt two mazes were used to determine whether female preference was related to male learning ability. In addition, male body size and saturation of the orange patches were measured. Female preference was found to be related to rate of learning, such that males that learnt the mazes faster were found to be more attractive to females, but was not found to be related to body size or saturation.