Intrinsic reproductive isolation between Trinidadian populations of the guppy, Poecilia reticulata

Although Trinidadian populations of the guppy, Poecilia reticulata, show considerable adaptive genetic differentiation, they have been assumed to show little or no reproductive isolation. We tested this assumption by crossing Caroni (Tacarigua River) and Oropuche (Oropuche R.) drainage populations from Trinidad's Northern Range, and by examining multiple aspects of reproductive compatibility in the F1, F2 and BC1 generations. In open-aquarium experiments, F1 males performed fewer numbers of mating behaviours relative to parental population controls. This is the first documentation of hybrid behavioural sterility within a species, and it suggests that such sterility may feasibly be involved in causing speciation. The crosses also uncovered hybrid breakdown for embryo viability, brood size and sperm counts. In contrast, no reductions in female fertility were detected, indicating that guppies obey Haldane's rule for sterility. Intrinsic isolation currently presents a much stronger obstacle to gene flow than behavioural isolation, and our results indicate that Trinidadian populations constitute a useful model for investigating incipient speciation.     

Structure and allometry of genitalia in males and females of a social African ground squirrel with high polygynandry

The few studies that have looked at genital allometry in mammals have typically shown a positively allometric relationship with body size and high coefficients of variation. Cryptic female choice, sexual conflict or sperm competition are mechanisms underlying genital evolution and as these are not mutually exclusive, they are often difficult to disentangle. In addition, these mechanisms are affected by both male and female social structure and/or mating strategies and, as such, pre- and post-copulatory behaviours have been shown to alter selection on genitalia. We examined genital traits and allometry in a polygynandrous and social ground squirrel Xerus inauris . We found that male testes are positively allometric and account for 1.5% of their body weight, one of the highest percentages known for sciurids. The penis, at 42.4% of head/body length, was isometric while the female reproductive tract, 22.4% head/body length, demonstrated no such relationship. Based on the allometric relationships of both males and females presented here, in conjunction with high levels of competition for females and lack of male aggression and territoriality, we suggest that sperm competition is the most likely mechanism for the evolution of the extremely large genitalia in this species.     

Sex differences in the trade-off between feeding and mating in the guppy

Male guppies Poecilia reticulata court almost continuously and often indulge in sneaky mating attempts. Female guppies, on the other hand, devote much of their time to foraging. This paper demonstrates that both sexes reduce their feeding rate in mixed-sex groups relative to single sex ones and suggests that the decrease is less pronounced for females than for males. Thus males make feeding and mating decisions that are dependent on hunger while female foraging behaviour is constrained by sexual harassment. The observed sex differences in behaviour are a consequence of asymmetrical mating costs in males and females.     

Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait

Although conspicuous visual sexual signals, such as bright colors,in males serve to attract females in numerous species, theymay also attract the attention of potential predators and thusmay be costly in terms of increasing individual risk of mortalityto predation. Most models of the evolution of extravagant malesexual traits and female preferences for them assume that thesexually preferred male trait is costly to produce and maintain.However, there is surprisingly little empirical evidence fordirect fitness costs associated with sexually selected visualtraits that enhance male mating success. In the present study,we report a direct fitness cost for sexually selected, brightbody-color patterns in males in the form of an associated greaterrisk of mortality to predation. By using the guppy (Poeciliareticulata) and the blue acara cichlid fish (Aequidens pulcher)as a model prey–predator system, we demonstrate experimentallythat individual cichlids preferentially and consistently approached,attacked, and captured the more brightly colored of two size-matchedmale guppies presented simultaneously in staged encounters.This resulted in the brightly colored male incurring, on average,a significantly higher risk of mortality given an encounterwith the predator than with the drabber male in matched pairs.Our results constitute strong behavioral evidence for a directviability cost associated with bright coloration in male guppies,and they corroborate the generally accepted paradigm that directionalpredation by visual fish predators against brightly colored,adult male guppies underlies the evolution of the known divergentcolor patterns in natural guppy populations that experiencedifferent intensities of predation. The viability cost associatedwith bright conspicuous coloration in male guppies potentiallyreinforces for females the reliability of this sexually selectedtrait as an indicator trait of male quality.     

Evolution of male and female genitalia following release from sexual selection

Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.     

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the ‘one‐size‐fits‐all’ hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One‐size‐fits‐all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One‐size‐fits‐all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.     

Population differentiation in Trinidadian guppies (Poecilia reticulata): patterns and problems

Populations of the guppy, Poecilia reficulata , in N. Trinidad exhibit marked population differentiation in allozyme frequencies. Here we investigate six further populations electrophoretically at 25 enzyme-coding loci to examine patterns in geographical structuring, genotypic distributions and genetic diversity. With one exception, possibly related to an experimental introduction, populations divided broadly (dendrogram of Nei's mean genetic identity, Ī) in accordance with proposed ancestral colonization. Most populations were in Hardy Weinberg equilibrium, though some significant deficits in heterozygotes were detected. Incorporating information from published data, markedly hjgher levels of genetic diversity (mean observed heterozygosity, _o) were recorded in lowland [_o= 0.0382 ± k0406 ( s.e .), n = 9] compared with upstream populations [_o= 0.0112 ± 00034 (S.E.), n = 9]. Patterns are discussed in relation to historical and present-day evolutionary forces.     

Characterization of tetranucleotide microsatellite markers in guppy (Poecilia reticulata)

Ten tetranucleotide microsatellite loci are characterized for guppy, Poecilia reticulata, an important model species in the study of adaptation and mating systems. Loci were isolated following a microsatellite enrichment procedure using probe‐labelled magnetic beads. These microsatellites were designed for use in examining gene flow, reproductive isolation, and parentage within natural guppy populations.     

Isolation and the development of shoaling in two populations of the guppy

Socially reared guppies Poecilia reticulata derived from two wild populations (Upper and Lower Aripo River, Trinidad) showed a significant relationship between body size and shoaling tendency, measured as the proportion of time spent in proximity to a bottle containing conspecifics. Larger females shoaled significantly more than smaller females. Fish from the high-shoaling population (Lower Aripo) showed significantly less shoaling behaviour when reared in isolation. In contrast, low-shoaling fish (Upper Aripo) demonstrated no significant change in their shoaling behaviour in response to social isolation.     

The function and evolution of male and female genitalia in Phyllophaga Harris scarab beetles (Coleoptera: Scarabaeidae)

Genitalia diversity in insects continues to fuel investigation of the function and evolution of these dynamic structures. Whereas most studies have focused on variation in male genitalia, an increasing number of studies on female genitalia have uncovered comparable diversity among females, but often at a much finer morphological scale. In this study, we analysed the function and evolution of male and female genitalia in Phyllophaga scarab beetles, a group in which both sexes exhibit genitalic diversity. To document the interaction between male and female structures during mating, we dissected flash‐frozen mating pairs from three Phyllophaga species and investigated fine‐scale morphology using SEM. We then reconstructed ancestral character states using a species tree inferred from mitochondrial and nuclear loci to elucidate and compare the evolutionary history of male and female genitalia. Our dissections revealed an interlocking mechanism of the female pubic process and male parameres that appears to improve the mechanical fit of the copulatory position. The comparative analyses, however, did not support coevolution of male and female structures and showed more erratic evolution of the female genitalia relative to males. By studying a group that exhibits obvious female genitalic diversity, we were able to demonstrate the relevance of female reproductive morphology in studies of male genital diversity.     

Schooling preferences for familiar fish in the guppy, Poecilia reticulata

Although schooling behaviour is an important antipredator response of guppies ( Poecilia reticulata ) in Trinidad it is not known whether fish elect to school with particular individuals. Familiarity is a simple mechanism that could lead to non-random associations within schools. In this paper we test the idea that prior experience of particular individuals influences the choice of partners during schooling. We show (in a laboratory study) that female guppies prefer to associate with familiar individuals. However, we are unable to detect any schooling preference for unfamiliar females from the same population.     

Using adaptive traits to consider potential consequences of temporal variation in selection: male guppy colour through time and space

Temporal variation in selection is typically evaluated by estimating and comparing selection coefficients in natural populations. Meta‐analyses of these coefficients have yielded important insights, but selection coefficients are limited in several respects, including low statistical power, imperfect fitness surrogates, and uncertainty regarding consequences for trait change. A complementary approach without these limitations is to examine temporal variation in adaptive traits themselves, which is mechanistically easier and more directly relevant to evolutionary consequences. We illustrate this approach by analyzing the colour patterns of male guppies, Poecilia reticulata, from each of six sites in Trinidad in each of 6 years. This system is particularly appropriate for our study because key aspects of colour variation are genetically‐based and responsive to selection. However, although spatial patterns of colour variation have been extensively considered in this system, no study has yet formally assessed annual temporal variation in non‐manipulated populations. Matching previous conclusions for the guppy system, we find that guppies from different sites manifest different colour patterns in association with different predation regimes. We here add the new finding that, although some temporal variation is present, spatial patterns of colour variation are generally consistent across years. These results suggest that, when considering adaptive traits, spatial variation is more important than temporal variation, although our study system might be exceptional in this regard. Additional studies examining spatiotemporal variation in adaptive traits could help to improve our understanding of the role that spatiotemporal variation in selection plays in the evolutionary process. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 108–122.     

Social transmission of maladaptive information in the guppy

Many animals are capable of learning from others, a processreferred to as social learning. There is little doubt that acapacity for social learning is an adaptation and that it typicallyresults in adaptive behavior. What is less clear is whetherthere are circumstances under which social learning can resultin the transmission of outdated, inappropriate, or maladaptiveinformation. Here we report an experimental study that investigatedthe social learning and transmission of maladaptive foraginginformation through small social groups of guppies, Poeciliareticulata. This experiment used a transmission chain designin which fish in small founder groups were trained to take eitheran energetically costly circuitous route to a feeder or a lesscostly short route, with trained founder members gradually replacedby untrained conspecifics. Three days after all the foundershad been removed, the behavioral traditions of groups of untrainedfish were still strongly influenced by their founder's behavior.Moreover, the rate at which untrained subjects that shoaledwith founder conspecifics trained to take the long route learnedto take the short route was significantly slower than for fishforaging alone. The results provide unequivocal evidence thatmaladaptive information can be socially transmitted throughanimal populations and imply that socially learned informationcan inhibit learning of the optimal behavior pattern.     

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, and fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H₂S containing) and nearby nonsulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation‐with‐gene‐flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.     

The form of sexual selection on male genitalia cannot be inferred from within-population variance and allometry - a case study in Aquarius remigis

Male genital morphology in insects and arachnids is characterized by static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits. The one-size-fits-all model of genital evolution attributes these patterns to stabilizing sexual selection. This model relies on the assumption that the observed patterns of variation and allometry reflect the form of sexual selection acting these traits. We test this by examining the patterns of scaling and trait variation for a set of genitalic and somatic morphological traits in male water striders (Aquarius remigis). This suite of traits is of particular interest because previous work has shown that the genitalic traits are under strong directional selection whereas the somatic traits are under either weak directional or stabilizing selection. Because the selection regime for these traits is known, we can, for the first time, test the purported relationship between trait variation, scaling, and the form of sexual selection. We show that the patterns of variation and scaling of these traits differ sharply from those predicted for traits experiencing strong directional sexual selection. Specifically, the male genital structures show static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits, in spite of consistent, strong, directional sexual selection. These scaling relationships and levels of variation are typical of genital traits in other insect species, where they have been presumed to reflect stabilizing sexual selection. Our data clearly refute the assumption of the one-size-fits-all hypothesis that hypoallometric scaling of genitalic traits implies stabilizing selection. We discuss the implications of this finding and propose future directions for improving our current understanding of genital evolution in arthropods.     

Parallel evolution and vicariance in the guppy (Poecilia reticulata) over multiple spatial and temporal scales

Well-studied model systems present ideal opportunities to understand the relative roles of contemporary selection versus historical processes in determining population differentiation and speciation. Although guppy populations in Trinidad have been a model for studies of evolutionary ecology and sexual selection for more than 50 years, this work has been conducted with little understanding of the phylogenetic history of this species. We used variation in nuclear (X-src) and mitochondrial DNA (mtDNA) sequences to examine the phylogeographic history of Poecilia reticulata Peters (the guppy) across its entire natural range, and to test whether patterns of morphological divergence are a consequence of parallel evolution. Phylogenetic, nested clade, population genetic, and demographic analyses were conducted to investigate patterns of genetic structure at several temporal scales and are discussed in relation to vicariant events, such as tectonic activity and glacial cycles, shaping northeast South American river drainages. The mtDNA phylogeny defined five major lineages, each associated with one or more river drainages, and analysis of molecular variance also detected geographic structuring among these river drainages in an evolutionarily conserved nuclear (X-src) locus. Nested clade and other demographic analyses suggest that the eastern Venezuela/ western Trinidad region is likely the center of origin of P. reticulata. Mantel tests show that the divergence of morphological characters, known to differentiate on a local scale in response to natural and sexual selection pressures, is not associated with mtDNA genetic distance; however, TreeScan analysis identified several significant associations of these characters with the haplotype tree. Parallel upstream/downstream patterns of morphological adaptation in response to selection pressures reported in P. reticulata within Trinidad rivers appears to persist across the natural range. Our results together with previous studies suggest that, although morphological variation in P. reticulata is primarily attributed to selection, phylogeographic history may also play a role.     

Ultraviolet vision and mate choice in the guppy (Poecilia reticulata)

Ultraviolet (UV) vision is well documented for many speciesof vertebrates. UV cues are known to be used in foraging, navigationand in mate choice. We conducted a series of behavioral experimentsto investigate the role of UV perception in mate choice inboth female and male guppies (Poecilia reticulata). In ourexperiments the visual appearance of potential mates was manipulatedusing either UV transmitting (UV+) or UV blocking (UV-) filters.Female guppies significantly preferred UV+ males. Male guppiestended to prefer UV- females, but their preferences were marginallynonsignificant. Further experiments investigating the roleof luminance, indicate that UV wavelengths are probably beingused for color discrimination rather than for detecting differencesin brightness. These experiments raise the possibility thatUV is used in mate assessment in different ways by male andfemale guppies. This may reflect the different strategies thatthe two sexes have in order to maximize reproductive success.To our knowledge, these are the first data showing that UVis used by any fish species in mate selection.     

Heterosis for neonatal survival in the guppy

Neonatal survival rate ranged from 91.8 to 100.0% in 12 populations of the guppy Poecilia reticulata , and was higher in naturalized Japanese stream populations than in domestic strains. Mean heterozygosity at five allozyme and four microsatellite loci varied between 0.112 and 0.430 and was significantly correlated with neonatal survival rate among populations, suggest ing that inbreeding decreases neonatal survival. Diallel and reciprocal crosses among four domestic strains demonstrated heterosis for neonatal survival. These results indicate that neonatal survival is genetically affected by heterosis and its antithesis, inbreeding depression. The relationship between neonatal survival and the mean heterozygosity suggests that overall heterozygosity is important for neonatal survival of the guppy.     

Geographical variation in allometry in the guppy (Poecilia reticulata)

Variation in static allometry, the power relationship between character size and body size among individuals at similar developmental stages, remains poorly understood. We tested whether predation or other ecological factors could affect static allometry by comparing the allometry between the caudal fin length and the body length in adult male guppies (Poecilia reticulata) among populations from different geographical areas, exposed to different predation pressures. Neither the allometric slopes nor the allometric elevations (intercept at constant slope) changed with predation pressure. However, populations from the Northern Range in Trinidad showed allometry with similar slopes but lower intercepts than populations from the Caroni and the Oropouche drainages. Because most of these populations are exposed to predation by the prawn Macrobrachium crenulatum, we speculated that the specific selection pressures exerted by this predator generated this change in relative caudal fin size, although effects of other environmental factors could not be ruled out. This study further suggests that the allometric elevation is more variable than the allometric slope.     

Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata)

Predators are widely assumed to create selection that shapes the evolution of prey escape abilities. However, this assumption is difficult to test directly due to the challenge of recording both predation and its evolutionary consequences in the wild. We examined these events by studying natural and experimental populations of Trinidadian guppies, Poecilia reticulata, which occur in distinct high-predation and low-predation environments within streams. Importantly, in the last two decades several populations of guppies have been experimentally introduced from one type of predatory environment into the other, allowing measurements of the consequences of change. We used this system to test two hypotheses: First, that changes in predatory environments create phenotypic selection favoring changes in escape ability of guppies, and second, that this selection can result in rapid evolution. For the first test we compared escape ability of wild caught guppies from high- versus low-predation environments by measuring survival rates during staged encounters with a major predator, the pike cichlid Crenicichla alta. We used guppies from three streams, comparing two within-stream pairs of natural populations and three within-stream pairs of an introduced population versus its natural source population. In every comparison, guppies from the high-predation population showed higher survival. These multiple, parallel divergences in guppy survival phenotype suggest that predatory environment does create selection of escape ability. We tested our second hypothesis by rearing guppies in common garden conditions in the laboratory, then repeating the earlier experiments using the F2 generation. As before, each comparison resulted in higher survival of guppies descended from the high-predation populations, demonstrating that population differences in escape ability have a genetic basis. These results also show that escape ability can evolve very rapidly in nature, that is, within 26-36 generations in the introduced populations. Interestingly, we found rapid evolutionary loss of escape ability in populations introduced into low-predation environments, suggesting that steep fitness trade-offs may influence the evolution of escape traits.