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BACKGROUND: Recent increases in understanding the ecological and evolutionary roles of microbial communities have underscored the importance of their hosts' biology. Yet, little is known about gut microbiota dynamics during the early stages of ecological diversification and speciation. We sequenced the V4 region of the 16s rRNA gene to study the gut microbiota of Nicaraguan Midas cichlid fish (Amphilophus cf. citrinellus). Specifically, we tested the hypothesis that parallel divergence in trophic ecology in extremely young adaptive radiations from two crater lakes is associated with parallel changes of their gut microbiota. RESULTS: Bacterial communities of fish guts and lake water were highly distinct, indicating that the gut microbiota is shaped by host-specific factors. Among individuals of the same crater lake, differentiation in trophic ecology was weakly associated with gut microbiota differentiation, suggesting that diet, to some extent, affects the gut microbiota. However, differences in trophic ecology were much more pronounced across than within species whereas similar patterns were not observed for taxonomic and functional differences of the gut microbiota. Across the two crater lakes, we could not detect conclusive evidence for parallel changes of the gut microbiota associated with trophic ecology. CONCLUSIONS: A lack of clearly differentiated niches during the early stages of ecological diversification might result in non-parallel changes of gut microbial communities, as observed in our study system as well as in other recently diverged fish species. Video Abstract.

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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.

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Freshwater sulfide springs have extreme environmental conditions that only few vertebrate species can tolerate. These species often develop a series of morphological and molecular adaptations to cope with the challenges of life under the toxic and hypoxic conditions of sulfide springs. In this paper, we described a new fish species of the genus Jenynsia, Anablepidae, from a sulfide spring in Northwestern Argentina, the first in the family known from such extreme environment. Jenynsia sulfurica n. sp. is diagnosable by the lack of scales on the pre-pelvic area or the presence of a single row of scales, continuous or not, from the isthmus to the bases of the pelvic fins. Additionally, it presents a series of morphological and molecular characteristics that appear convergent with those seen in other fish species (e.g., Poeciliids) inhabiting sulfide springs. Most notably, J. sulfurica has an enlarged head and postorbital area compared to other fish of the genus and a prognathous lower jaw with a hypertrophied lip, thought to facilitate respiration at the air-water interface. Analyses of cox1 sequence showed that J. sulfurica has two unique mutations resulting in amino acid substitutions convergent to those seen in Poeciliids from sulfide springs and known to provide a physiological mechanism related to living in sulfide environments. A phylogenetic analysis, including molecular and morphological characters, placed J. sulfurica as sister taxa to J. alternimaculata, a species found in nearby, non-sulfide habitats directly connected to the sulfide springs. Thus, it can be inferred that the selection imposed by the presence of H2S has resulted in the divergence between these two species and has potentially served as a barrier to gene flow.

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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.

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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.

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Large-scale infrastructure projects commonly have large effects on the environment. The planned construction of the Nicaragua Canal will irreversibly alter the aquatic environment of Nicaragua in many ways. Two distinct drainage basins (San Juan and Punta Gorda) will be connected and numerous ecosystems will be altered. Considering the project's far-reaching environmental effects, too few studies on biodiversity have been performed to date. This limits provision of robust environmental impact assessments. We explored the geographic distribution of taxonomic and genetic diversity of freshwater fish species (Poecilia spp., Amatitlania siquia, Hypsophrys nematopus, Brycon guatemalensis, and Roeboides bouchellei) across the Nicaragua Canal zone. We collected population samples in affected areas (San Juan, Punta Gorda, and Escondido drainage basins), investigated species composition of 2 drainage basins and performed genetic analyses (genetic diversity, analysis of molecular variance) based on mitochondrial cytb. Freshwater fish faunas differed substantially between drainage basins (Jaccard similarity = 0.33). Most populations from distinct drainage basins were genetically differentiated. Removing the geographic barrier between these basins will promote biotic homogenization and the loss of unique genetic diversity. We found species in areas where they were not known to exist, including an undescribed, highly distinct clade of live bearing fish (Poecilia). Our results indicate that the Nicaragua Canal likely will have strong impacts on Nicaragua's freshwater biodiversity. However, knowledge about the extent of these impacts is lacking, which highlights the need for more thorough investigations before the environment is altered irreversibly.

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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.

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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.

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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.

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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.

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Deuterium isotope analyses have revolutionized the study of migratory connectivity because global gradients of deuterium in precipitation (deltaD(P)) are expressed on a continental scale. Several authors have constructed continental scale base maps of deltaD(P) to provide a spatial reference for studying the movement patterns of migratory species and, although they are very useful, these maps present a static, 40-year average view of the landscape that ignores much underlying inter-annual variation. To more fully understand the consequences of this underlying variation, we analyzed the GNIP deuterium data, the source for all current deltaD(P) maps, to estimate the minimum separation in deltaD(P) (and latitude) necessary to conclude with a given level of confidence that distinct deltaD(P) values represent different geographic sites. Extending analyses of deltaD(P) successfully to deuterium in tissues of living organisms, e.g., feathers in migratory birds (deltaD(F)), is dependent on the existence of geographic separation of deltaD(P), where every geographic location has a distribution of values associated with temporal variability in deltaD(P). Analyses were conducted for three distinct geographic regions: North America, eastern North America (east of longitude 100 degrees W), and Argentina. At the 80% confidence level, the minimum separation values were 12, 7, and 14 degrees of latitude (equivalent to 53, 31, and 32 per thousand) for North America, eastern North America, and Argentina, respectively. Hence, in eastern North America, for example, one may not be able to accurately assign individual samples to sites separated by less than about 7 degrees of latitude as the distributions of deltaD(P) were not distinct at latitudes <7 degrees apart. Moreover, two samples that differ by less than 31 per thousand cannot be confidently said to originate from different latitudes. These estimates of minimum separation for deltaD(P) do not include other known sources of variation in feather deuterium (deltaD(F)) and hence are a first order approximation that may be useful, in the absence of more specific information for the system of interest, for planning and interpreting the results of new stable isotope studies.

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