Trophic niche drives the evolution of craniofacial shape in Trinidadian guppies.

Diverse clades of fishes adapted to feeding on the benthos repeatedly converge on steep craniofacial profiles and shorter, wider heads. But in an incipient radiation, to what extent is this morphological evolution measurable and can we distinguish the relative genetic vs. plastic effects? We use the Trinidadian guppy (Poecilia reticulata) to test the repeatability of adaptation and the alignment of genetic and environmental effects shaping poecilid craniofacial morphology. We compare wild-caught and common garden lab-reared fish to quantify the genetic and plastic components of craniofacial morphology across 4 populations from 2 river drainage systems (n = 56 total). We first use micro-computed tomography to capture 3D morphology, then place both landmarks and semilandmarks to perform size-corrected 3D morphometrics and quantify shape space. We find a measurable, significant, and repeatable divergence in craniofacial shape between high-predation invertivore and low-predation detritivore populations. As predicted from previous examples of piscine adaptive trophic divergence, we find increases in head slope and craniofacial compression among the benthic detritivore foragers. Furthermore, the effects of environmental plasticity among benthic detritivores produce exaggerated craniofacial morphological change along a parallel axis to genetic morphological adaptation from invertivore ancestors. Overall, many of the major patterns of benthic-limnetic craniofacial evolution appear convergent among disparate groups of teleost fishes.

Repeated independent origins of the placenta reveal convergent and divergent organ evolution within a single fish family (Poeciliidae).

An outstanding question in biology is to what extent convergent evolution produces similar, but not necessarily identical, complex phenotypic solutions. The placenta is a complex organ that repeatedly evolved in the livebearing fish family Poeciliidae. Here, we apply comparative approaches to test whether evolution has produced similar or different placental phenotypes in the Poeciliidae and to what extent these phenotypes correlate with convergence at the molecular level. We show the existence of two placental phenotypes characterized by distinctly different anatomical adaptations (divergent evolution). Furthermore, each placental phenotype independently evolved multiple times across the family, providing evidence for repeated convergence. Moreover, our comparative genomic analysis revealed that the genomes of species with different placentas are evolving at a different pace. Last, we show that the two placental phenotypes correlate with two previously described contrasting life-history optima. Our results argue for high evolvability (both divergent and convergent) of the placenta within a group of closely related species in a single family.

How to generate and test hypotheses about colour: insights from half a century of guppy research.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Female preference for rare males is maintained by indirect selection in Trinidadian guppies.

When females prefer mates with rare phenotypes, sexual selection can maintain rather than deplete genetic variation. However, there is no consensus on why this widespread and frequently observed preference might evolve and persist. We examine the fitness consequences of female preference for rare male color patterns in a natural population of Trinidadian guppies, using a pedigree that spans 10 generations. We demonstrate (i) a rare male reproductive advantage, (ii) that females that mate with rare males gain an indirect fitness advantage through the mating success of their sons, and (iii) the fitness benefit that females accrue through their "sexy sons" evaporates for their grandsons as their phenotype becomes common. Counter to prevailing theory, we show that female preference can be maintained through indirect selection.

Visual Background Choice and Light Environment Affect Male Guppy Visual Contrast.

Male guppies (Poecilia reticulata) have multiple colored spots and perform courtship displays near the edges of streams in Trinidad in shallow water flowing through rainforest. Depending upon the orientation of the pair, the female sees the male displays against gravel or other stream bed substrates or against the spacelight-the roughly uniform light coming from the water column away from the bank. We observed courting pairs in two adjacent natural streams and noted the directions of each male display. We found that the female sees the male more often against spacelight than against gravel when females either faced the spacelight from the opposite bank or from downstream, or both. Visual modelling using natural substrate reflectances and field light measurements showed higher chromatic contrast of males against spacelight than against substrates independent of the two ambient light environments used during displays, but achromatic contrast depended upon the ambient light habitat. This suggests that courtship involves both chromatic and achromatic contrast. We conclude that the orientation of courting pairs and the ambient light spectrum should be accounted for in studies of mate choice, because the visual background and light affect visibility, and these differ with orientation.

Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata).

Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome-wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.

Life histories as mosaics: Plastic and genetic components differ among traits that underpin life-history strategies.

Life-history phenotypes emerge from clusters of traits that are the product of genes and phenotypic plasticity. If the impact of the environment differs substantially between traits, then life histories might not evolve as a cohesive whole. We quantified the sensitivity of components of the life history to food availability, a key environmental difference in the habitat occupied by contrasting ecotypes, for 36 traits in fast- and slow-reproducing Trinidadian guppies. Our dataset included six putatively independent origins of the slow-reproducing, derived ecotype. Traits varied substantially in plastic and genetic control. Twelve traits were influenced only by food availability (body lengths, body weights), five only by genetic differentiation (interbirth intervals, offspring sizes), 10 by both (litter sizes, reproductive timing), and nine by neither (fat contents, reproductive allotment). Ecotype-by-food interactions were negligible. The response to low food was aligned with the genetic difference between high- and low-food environments, suggesting that plasticity was adaptive. The heterogeneity among traits in environmental sensitivity and genetic differentiation reveals that the components of the life history may not evolve in concert. Ecotypes may instead represent mosaics of trait groups that differ in their rate of evolution.

Differential habitat use and recruitment facilitate coexistence in a community with intraguild predation.

Theory predicts that species engaged in intraguild predation (IGP) can only coexist under limited conditions, yet IGP is common in nature. Habitat complexity can promote coexistence by reducing encounter rates, but little information is known about the contribution of differential habitat use. We hypothesized that differential use of alternative habitats promotes coexistence of an intraguild (IG) predator and prey. We evaluated predictions of this hypothesis with an experimental introduction of an IG predator fish into four natural stream communities that previously contained only the IG prey fish. We monitored the development of this IGP over the course of four years to determine how each species used alternative stream habitats. The introduced species preferred pool habitats while the resident species was more evenly distributed across pools and riffles. The density of the resident decreased in the pool habitat preferred by the invader, accompanied by a local increase in the mean of the resident size distribution. Selective predation by the invader on hatchling residents appears to impact the residents' demographic response. The continued recruitment of resident juveniles in riffles, where the introduced species is rare, facilitated the persistence of the resident. This differential use of habitats was not accompanied by a change in the resident's growth rates in either habitat. Our results showed that differential habitat selection and recruitment promoted persistence during an invasion involving IGP, which helps to bridge the gap between theory and observation in explaining coexistence in IGP systems.

The experimental range extension of guppies (Poecilia reticulata) influences the metabolic activity of tropical streams.

The ecological consequences of biological range extensions reflect the interplay between the functional characteristics of the newly arrived species and their recipient ecosystems. Teasing apart the relative contribution of each component is difficult because most colonization events are studied retrospectively, i.e., after a species became established and its consequences apparent. We conducted a prospective experiment to study the ecosystem consequences of a consumer introduction, using whole-stream metabolism as our integrator of ecosystem activity. In four Trinidadian streams, we extended the range of a native fish, the guppy (Poecilia reticulata), by introducing it over barrier waterfalls that historically excluded it from these upper reaches. To assess the context dependence of these range extensions, we thinned the riparian forest canopy on two of these streams to increase benthic algal biomass and productivity. Guppy's range extension into upper stream reaches significantly impacted stream metabolism but the effects depended upon the specific stream into which they had been introduced. Generally, increases in guppy biomass caused an increase in gross primary production (GPP) and community respiration (CR). The effects guppies had on GPP were similar to those induced by increased light level and were larger in strength than the effects stream stage had on CR. These results, combined with results from prior experiments, contribute to our growing understanding of how consumers impact stream ecosystem function when they expand their range into novel habitats. Further study will reveal whether local adaptation, known to occur rapidly in these guppy populations, modifies the ecological consequences of this species introduction.

The evolution of the placenta in poeciliid fishes.

How and why complex organs evolve is generally lost to history. The mammalian placenta, for example, was derived from a single common ancestor that lived over 100 million years ago.1-3 Therefore, the selective factors favoring this complex trait remain obscure. Species in the live-bearing fish family Poeciliidae have independently evolved placentas numerous times while retaining closely related non-placental sister species.4-7 This provides the raw material to test alternative hypotheses for the evolution of the placenta. We assemble an extensive species-level dataset on reproductive mode, life histories, and habitat, and then implement phylogenetic comparative methods to test adaptive hypotheses for the evolution of the placenta. We find no consistent family-wide associations between placentation and habitat. However, placental species exhibit significantly reduced reproductive allotment and have a higher likelihood of exhibiting superfetation (the ability to gestate multiple broods at different developmental stages). Both features potentially increase body streamlining and enhance locomotor performance during pregnancy, possibly providing selective advantage in performance-demanding environments such as those with high predation or fast water flow. Furthermore, we found significant interactions between body size and placentation for offspring size and fecundity. Relative to non-placental species, placentation is associated with higher fecundity and smaller offspring size in small-bodied species and lower fecundity and larger offspring size in large-bodied species. This pattern suggests that there may be two phenotypic adaptive peaks, corresponding to two selective optima, associated with placentation: one represented by small-bodied species that have fast life histories, and the second by large-bodied species with slow life histories.

Parallel Genomic Changes Drive Repeated Evolution of Placentas in Live-Bearing Fish.

The evolutionary origin of complex organs challenges empirical study because most organs evolved hundreds of millions of years ago. The placenta of live-bearing fish in the family Poeciliidae represents a unique opportunity to study the evolutionary origin of complex organs, because in this family a placenta evolved at least nine times independently. It is currently unknown whether this repeated evolution is accompanied by similar, repeated, genomic changes in placental species. Here, we compare whole genomes of 26 poeciliid species representing six out of nine independent origins of placentation. Evolutionary rate analysis revealed that the evolution of the placenta coincides with convergent shifts in the evolutionary rate of 78 protein-coding genes, mainly observed in transporter- and vesicle-located genes. Furthermore, differences in sequence conservation showed that placental evolution coincided with similar changes in 76 noncoding regulatory elements, occurring primarily around genes that regulate development. The unexpected high occurrence of GATA simple repeats in the regulatory elements suggests an important function for GATA repeats in developmental gene regulation. The distinction in molecular evolution observed, with protein-coding parallel changes more often found in metabolic and structural pathways, compared with regulatory change more frequently found in developmental pathways, offers a compelling model for complex trait evolution in general: changing the regulation of otherwise highly conserved developmental genes may allow for the evolution of complex traits.

Towards a more precise - and accurate - view of eco-evolution.

Over the past 15 years, the number of papers focused on 'eco-evo dynamics' has increased exponentially (Figure 1). This pattern suggests the rapid growth of a new, integrative discipline. We argue this overstates the case. First, the terms 'eco-evo dynamics' and 'eco-evo interactions' are used too imprecisely. As a result, many studies that claim to describe eco-evo dynamics are actually describing basic ecological or evolutionary processes. Second, these terms are often used as if the study of how ecological and evolutionary processes are intertwined is novel when, in fact, it is not. The result is confusion over what the term 'eco-evolution' and its derivatives describe. We advocate a more precise definition of eco-evolution that is more useful in efforts to understand and characterise the diversity of ecological and evolutionary processes and that focuses attention on the subset of those processes that occur only when ecological and evolutionary timescales are comparable. [Figure: see text].

Environmental Change, If Unaccounted, Prevents Detection of Cryptic Evolution in a Wild Population.

AbstractDetecting contemporary evolution requires demonstrating that genetic change has occurred. Mixed effects models allow estimation of quantitative genetic parameters and are widely used to study evolution in wild populations. However, predictions of evolution based on these parameters frequently fail to match observations. Here, we applied three commonly used quantitative genetic approaches to predict the evolution of size at maturity in a wild population of Trinidadian guppies. Crucially, we tested our predictions against evolutionary change observed in common-garden experiments performed on samples from the same population. We show that standard quantitative genetic models underestimated or failed to detect the cryptic evolution of this trait as demonstrated by the common-garden experiments. The models failed because (1) size at maturity and fitness both decreased with increases in population density, (2) offspring experienced higher population densities than their parents, and (3) selection on size was strongest at high densities. When we accounted for environmental change, predictions better matched observations in the common-garden experiments, although substantial uncertainty remained. Our results demonstrate that predictions of evolution are unreliable if environmental change is not appropriately captured in models.

Rapid evolution and plasticity of genitalia.

Genital morphology exhibits tremendous variation and is intimately linked with fitness. Sexual selection, nonmating natural selection and neutral forces have been explored as potential drivers of genital divergence. Though less explored, genitalia may also be plastic in response to the developmental environment. In poeciliid fishes, the length of the male intromittent organ, the gonopodium, may be driven by sexual selection if longer gonopodia attract females or aid in forced copulation attempts or by nonmating natural selection if shorter gonopodia allow predator evasion. The rearing environment may also affect gonopodium development. Using an experimental introduction of Trinidadian guppies into four replicate streams with reduced predation risk, we tested whether this new environment caused the evolution of genitalia. We measured gonopodium length after rearing the source and introduced populations for two generations in the laboratory to remove maternal and other environmental effects. We split full-sibling brothers into different rearing treatments to additionally test for developmental plasticity of gonopodia in response to predator cues and food levels as well as the evolution of plasticity. The introduced populations had shorter gonopodia after accounting for body size, demonstrating rapid genital evolution in 2-3 years (8-12 generations). Brothers reared on low food levels had longer gonopodia relative to body size than those on high food, reflecting maintenance of gonopodium length despite a reduction in body size. In contrast, gonopodium length was not significantly different in response to the presence or absence of predator cues. Because the plastic response to low food was maintained between the source and introduced populations, there was no evidence that plasticity evolved. This study demonstrates the importance of both evolution and developmental plasticity in explaining genital variation.

Novel parasite invasion leads to rapid demographic compensation and recovery in an experimental population of guppies.

The global movement of pathogens is altering populations and communities through a variety of direct and indirect ecological pathways. The direct effect of a pathogen on a host is reduced survival, which can lead to decreased population densities. However, theory also suggests that increased mortality can lead to no change or even increases in the density of the host. This paradoxical result can occur in a regulated population when the pathogen's negative effect on survival is countered by increased reproduction at the lower density. Here, we analyze data from a long-term capture-mark-recapture experiment of Trinidadian guppies (Poecilia reticulata) that were recently infected with a nematode parasite (Camallanus cotti). By comparing the newly infected population with a control population that was not infected, we show that decreases in the density of the infected guppy population were transient. The guppy population compensated for the decreased survival by a density-dependent increase in recruitment of new individuals into the population, without any change in the underlying recruitment function. Increased recruitment was related to an increase in the somatic growth of uninfected fish. Twenty months into the new invasion, the population had fully recovered to preinvasion densities even though the prevalence of infection of fish in the population remained high (72%). These results show that density-mediated indirect effects of novel parasites can be positive, not negative, which makes it difficult to extrapolate to how pathogens will affect species interactions in communities. We discuss possible hypotheses for the rapid recovery.

Individual differences determine the strength of ecological interactions.

Biotic interactions are central to both ecological and evolutionary dynamics. In the vast majority of empirical studies, the strength of intraspecific interactions is estimated by using simple measures of population size. Biologists have long known that these are crude metrics, with experiments and theory suggesting that interactions between individuals should depend on traits, such as body size. Despite this, it has been difficult to estimate the impact of traits on competitive ability from ecological field data, and this explains why the strength of biotic interactions has empirically been treated in a simplistic manner. Using long-term observational data from four different populations, we show that large Trinidadian guppies impose a significantly larger competitive pressure on conspecifics than individuals that are smaller; in other words, competition is asymmetric. When we incorporate this asymmetry into integral projection models, the predicted size structure is much closer to what we see in the field compared with models where competition is independent of body size. This difference in size structure translates into a twofold difference in reproductive output. This demonstrates how the nature of ecological interactions drives the size structure, which, in turn, will have important implications for both the ecological and evolutionary dynamics.

Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles.

Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi.

Predation risk shapes the degree of placentation in natural populations of live-bearing fish.

The placenta is a complex life-history trait that is ubiquitous across the tree of life. Theory proposes that the placenta evolves in response to high performance-demanding conditions by shifting maternal investment from pre- to post-fertilisation, thereby reducing a female's reproductive burden during pregnancy. We test this hypothesis by studying populations of the fish species Poeciliopsis retropinna in Costa Rica. We found substantial variation in the degree of placentation among natural populations associated with predation risk: females from high predation populations had significantly higher degrees of placentation compared to low predation females, while number, size and quality of offspring at birth remained unaffected. Moreover, a higher degree of placentation correlated with a lower reproductive burden and hence likely an improved swimming performance during pregnancy. Our study advances an adaptive explanation for why the placenta evolves by arguing that an increased degree of placentation offers a selective advantage in high predation environments.

Eco-Evolutionary Feedbacks Predict the Time Course of Rapid Life-History Evolution.

Organisms can change their environment and in doing so change the selection they experience and how they evolve. Population density is one potential mediator of such interactions because high population densities can impact the ecosystem and reduce resource availability. At present, such interactions are best known from theory and laboratory experiments. Here we quantify the importance of such interactions in nature by transplanting guppies from a stream where they co-occur with predators into tributaries that previously lacked both guppies and predators. If guppies evolve solely because of the immediate reduction in mortality rate, the strength of selection and rate of evolution should be greatest at the outset and then decline as the population adapts to its new environment. If indirect effects caused by the increase in guppy population density in the absence of predation prevail, then there should be a lag in guppy evolution because time is required for them to modify their environment. The duration of this lag is predicted to be associated with the environmental modification caused by guppies. We observed a lag in life-history evolution associated with increases in population density and altered ecology. How guppies evolved matched predictions derived from evolutionary theory that incorporates such density effects.

How conflict shapes evolution in poeciliid fishes.

In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation. Here we test these predictions of the viviparity driven conflict hypothesis (VDCH) in live-bearing poecilid fishes, a group showing multiple independent origins of placentation and extreme variation in male sexually selected traits. As predicted, male sexually selected traits are only gained in lineages that lack placentas; while there is little or no influence of male traits on the evolution of placentas. Both results are consistent with the mode of female provisioning governing the evolution of male attributes. Moreover, it is the presence of male sexually selected traits (pre-copulatory), rather than placentation (post-copulatory), that are associated with higher rates of speciation. These results highlight a causal interaction between female reproductive mode, male sexual selection and the rate of speciation, suggesting a role for conflict in shaping diverse aspects of organismal biology.