Julián Torres-Dowdall

Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata).

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.

Incipient sympatric speciation in Midas cichlid fish from the youngest and one of the smallest crater lakes in Nicaragua due to differential use of the benthic and limnetic habitats

Abstract Understanding how speciation can occur without geographic isolation remains a central objective in evolutionary biology. Generally, some form of disruptive selection and assortative mating are necessary for sympatric speciation to occur. Disruptive selection can arise from intraspecific competition for resources. If this competition leads to the differential use of habitats and variation in relevant traits is genetically determined, then assortative mating can be an automatic consequence (i.e., habitat isolation). In this study, we caught Midas cichlid fish from the limnetic (middle of the lake) and benthic (shore) habitats of Crater Lake Asososca Managua to test whether some of the necessary conditions for sympatric speciation due to intraspecific competition and habitat isolation are given. Lake As. Managua is very small (<900 m in diameter), extremely young (maximally 1245 years of age), and completely isolated. It is inhabited by, probably, only a single endemic species of Midas cichlids, Amphilophus tolteca. We found that fish from the limnetic habitat were more elongated than fish collected from the benthic habitat, as would be predicted from ecomorphological considerations. Stable isotope analyses confirmed that the former also exhibit a more limnetic lifestyle than the latter. Furthermore, split‐brood design experiments in the laboratory suggest that phenotypic plasticity is unlikely to explain much of the observed differences in body elongation that we observed in the field. Yet, neutral markers (microsatellites) did not reveal any genetic clustering in the population. Interestingly, demographic inferences based on RAD‐seq data suggest that the apparent lack of genetic differentiation at neutral markers could simply be due to a lack of time, as intraspecific competition may only have begun a few hundred generations ago.

Gene flow from an adaptively divergent source causes rescue through genetic and demographic factors in two wild populations of Trinidadian guppies

Genetic rescue, an increase in population growth owing to the infusion of new alleles, can aid the persistence of small populations. Its use as a management tool is limited by a lack of empirical data geared toward predicting effects of gene flow on local adaptation and demography. Experimental translocations provide an ideal opportunity to monitor the demographic consequences of gene flow. In this study we take advantage of two experimental introductions of Trinidadian guppies to test the effects of gene flow on downstream native populations. We individually marked guppies from the native populations to monitor population dynamics for 3 months before and 26 months after gene flow. We genotyped all individuals caught during the first 17 months at microsatellite loci to classify individuals by their genetic ancestry: native, immigrant, F1 hybrid, F2 hybrid, or backcross. Our study documents a combination of demographic and genetic rescue over multiple generations under fully natural conditions. Within both recipient populations, we found substantial and long‐term increases in population size that could be attributed to high survival and recruitment caused by immigration and gene flow from the introduction sites. Our results suggest that low levels of gene flow, even from a divergent ecotype, can provide a substantial demographic boost to small populations, which may allow them to withstand environmental stochasticity.

Parallelism Isn't Perfect: Could Disease and Flooding Drive a Life-History Anomaly in Trinidadian Guppies?

Nonparallel evolution, where independent populations occupy similar environments but show phenotypic differences, can uncover previously ignored selective factors. We investigated a nonparallelism in the life-history strategy of a Trinidadian guppy population, a system famous for parallel adaptation to differences in predation risk. We tested the hypothesis that high mortality drives an observed fast life-history pattern (i.e., earlier maturation and more frequent reproductive events) that is atypical for a low-predation environment. Using mark-recapture techniques, we compared neighboring low-predation populations, finding significantly higher mortality rates in the population with atypical life-history traits. Mortality was elevated during the wet season, when flooding was common. Moreover, individuals from the anomalous population were more likely to transition from healthy to infected disease states. Our results stand out against previous patterns observed in this system, indicating that higher mortality caused by disease and flooding may have selected for a faster life history. Thus, we highlight that even in systems famous for parallel adaptation, variation in selective pressures can result in nonparallel phenotypic evolution.

Ecological and lineage specific factors drive the molecular evolution of rhodopsin in cichlid fishes

The visual system in the colorful cichlid fishes from the African great lakes is believed to be important for their adaptive radiations. However, few studies have attempted to compare the visual system of radiating cichlid lineages with that of cichlids that have not undergone recent radiations. One such study published in this journal (Schott RK, Refvik SP, Hauser FE, López-Fernández H, Chang BSW. 2014. Divergent positive selection in rhodopsin from lake and riverine cichlid fishes. Mol Biol Evol. 31:1149-1165) found divergent selection on rhodopsin between African lacustrine and riverine cichlid species and riverine Neotropical cichlids, concluding that ecology drives the molecular evolution of this opsin. Here, we expand this analysis by incorporating rhodopsin sequences from Neotropical lacustrine cichlids and show that both ecology and phylogeny are important drivers of the molecular evolution of rhodopsin in cichlids. We found little overlap of sites under selection between African and Neotropical lineages and a faster rate of molecular evolution in African compared with Neotropical cichlids. These results support the notion that genetic or population genetic features particular to African cichlids contributed to their radiations.

Rapid and Parallel Adaptive Evolution of the Visual System of Neotropical Midas Cichlid Fishes

Midas cichlid fish are a Central American species flock containing 13 described species that has been dated to only a few thousand years old, a historical timescale infrequently associated with speciation. Their radiation involved the colonization of several clear water crater lakes from two turbid great lakes. Therefore, Midas cichlids have been subjected to widely varying photic conditions during their radiation. Being a primary signal relay for information from the environment to the organism, the visual system is under continuing selective pressure and a prime organ system for accumulating adaptive changes during speciation, particularly in the case of dramatic shifts in photic conditions. Here, we characterize the full visual system of Midas cichlids at organismal and genetic levels, to determine what types of adaptive changes evolved within the short time span of their radiation. We show that Midas cichlids have a diverse visual system with unexpectedly high intra- and interspecific variation in color vision sensitivity and lens transmittance. Midas cichlid populations in the clear crater lakes have convergently evolved visual sensitivities shifted toward shorter wavelengths compared with the ancestral populations from the turbid great lakes. This divergence in sensitivity is driven by changes in chromophore usage, differential opsin expression, opsin coexpression, and to a lesser degree by opsin coding sequence variation. The visual system of Midas cichlids has the evolutionary capacity to rapidly integrate multiple adaptations to changing light environments. Our data may indicate that, in early stages of divergence, changes in opsin regulation could precede changes in opsin coding sequence evolution.

Incipient speciation driven by hypertrophied lips in Midas cichlid fishes

Sympatric speciation has been debated in evolutionary biology for decades. Although it has gained in acceptance recently, still only a handful of empirical examples are seen as valid (e.g. crater lake cichlids). In this study, we disentangle the role of hypertrophied lips in the repeated adaptive radiations of Nicaraguan crater lake cichlid fish. We assessed the role of disruptive selection and assortative mating during the early stages of divergence and found a functional trade‐off in feeding behaviour between thick‐ and thin‐lipped ecotypes, suggesting that this trait is a target of disruptive selection. Thick‐lipped fish perform better on nonevasive prey at the cost of a poorer performance on evasive prey. Using enclosures in the wild, we found that thick‐lipped fish perform significantly better in rocky than in sandy habitats. We found almost no mixed pairs during two breeding seasons and hence significant assortative mating. Genetic differentiation between ecotypes seems to be related to the time since colonization, being subtle in L. Masaya (1600 generations ago) and absent in the younger L. Apoyeque (<600 generations ago). Genome‐wide differentiation between ecotypes was higher in the old source lakes than in the young crater lakes. Our results suggest that hypertrophied lips might be promoting incipient sympatric speciation through divergent selection (ecological divergence in feeding performance) and nonrandom mating (assortative mating) in the young Nicaraguan crater lakes. Nonetheless, further manipulative experiments are needed in order to confirm the role of hypertrophied lips as the main cue for assortative mating.

Phenotypic plasticity changes correlations of traits following experimental introductions of Trinidadian guppies (Poecilia reticulata).

Colonization of novel environments can alter selective pressures and act as a catalyst for rapid evolution in nature. Theory and empirical studies suggest that the ability of a population to exhibit an adaptive evolutionary response to novel selection pressures should reflect the presence of sufficient additive genetic variance and covariance for individual and correlated traits. As correlated traits should not respond to selection independently, the structure of correlations of traits can bias or constrain adaptive evolution. Models of how multiple correlated traits respond to selection often assume spatial and temporal stability of trait-correlations within populations. Yet, trait-correlations can also be plastic in response to environmental variation. Phenotypic plasticity, the ability of a single genotype to produce different phenotypes across environments, is of particular interest because it can induce population-wide changes in the combination of traits exposed to selection and change the trajectory of evolutionary divergence. We tested the ability of phenotypic plasticity to modify trait-correlations by comparing phenotypic variance and covariance in the body-shapes of four experimental populations of Trinidadian guppies (Poecilia reticulata) to their ancestral population. We found that phenotypic plasticity produced both adaptive and novel aspects of body-shape, which was repeated in all four experimental populations. Further, phenotypic plasticity changed patterns of covariance among morphological characters. These findings suggest our ability to make inferences about patterns of divergence based on correlations of traits in extant populations may be limited if novel environments not only induce plasticity in multiple traits, but also change the correlations among the traits.

Rapid adaptation to a novel light environment: the importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.)

Colonization of novel habitats is typically challenging to organisms. In the initial stage after colonization, approximation to fitness optima in the new environment can occur by selection acting on standing genetic variation, modification of developmental patterns or phenotypic plasticity. Midas cichlids have recently colonized crater Lake Apoyo from great Lake Nicaragua. The photic environment of crater Lake Apoyo is shifted towards shorter wavelengths compared to great Lake Nicaragua and Midas cichlids from both lakes differ in visual sensitivity. We investigated the contribution of ontogeny and phenotypic plasticity in shaping the visual system of Midas cichlids after colonizing this novel photic environment. To this end, we measured cone opsin expression both during development and after experimental exposure to different light treatments. Midas cichlids from both lakes undergo ontogenetic changes in cone opsin expression, but visual sensitivity is consistently shifted towards shorter wavelengths in crater lake fish, which leads to a paedomorphic retention of their visual phenotype. This shift might be mediated by lower levels of thyroid hormone in crater lake Midas cichlids (measured indirectly as dio2 and dio3 gene expression). Exposing fish to different light treatments revealed that cone opsin expression is phenotypically plastic in both species during early development, with short and long wavelength light slowing or accelerating ontogenetic changes, respectively. Notably, this plastic response was maintained into adulthood only in the derived crater lake Midas cichlids. We conclude that the rapid evolution of Midas cichlids’ visual system after colonizing crater Lake Apoyo was mediated by a shift in visual sensitivity during ontogeny and was further aided by phenotypic plasticity during development.

Gene Flow Constrains and Facilitates Genetically Based Divergence in Quantitative Traits

Theory predicts that gene flow will decrease phenotypic differences among populations. Correlational studies have in some cases documented constraining effects of gene flow on phenotypic divergence and/or have also provided evidence for local differentiation despite high gene flow. However, correlative studies are unable to evaluate how gene flow affects genetically based phenotypic divergence or the extent to which gene flow constrains adaptive divergence. Translocation experiments using Trinidadian guppies provided an opportunity to test the effects of new gene flow on quantitative traits in native recipient populations. We measured a suite of traits in guppies reared in common garden environments before and multiple generations following gene flow from guppies that originated from a different environment. We interpreted our results in light of a priori predictions based on evolutionary theory and extensive background information about guppies and our focal populations. Although we could not include a spatiotemporal control that would allow us to be certain that the observed changes were directly caused by gene flow, we found that post-gene flow populations showed genetically based shifts in most traits. Whether traits shifted in predicted adaptive directions or whether they became more or less similar to the source population depended on the trait and initial conditions of the population. Our study provided a rare opportunity to test how recent gene flow affects genetically based changes in traits with known adaptive significance, and our results attest to the complex interactions between gene flow and selection.