Colonization Of Novel Environments Research Articles

Phenotypic plasticity in tropical butterflies is linked to climatic seasonality on a macroevolutionary scale.

Phenotypic plasticity can be adaptive in fluctuating environments by providing rapid environment-phenotype matching and this applies particularly in seasonal environments. African Bicyclus butterflies have repeatedly colonized seasonal savannahs from ancestral forests around the late Miocene, and many species now exhibit seasonal polyphenism. On a macroevolutionary scale, it can be expected that savannah species will exhibit higher plasticity because of experiencing stronger environmental seasonality than forest species. We quantified seasonality using environmental niche modeling and surveyed the degree of plasticity in a key wing pattern element (eyespot size) using museum specimens. We showed that species occurring in highly seasonal environments display strong plasticity, while species in less seasonal or aseasonal environments exhibit surprisingly variable degrees of plasticity, including strong to no plasticity. Furthermore, eyespot size plasticity has a moderate phylogenetic signal and the ancestral Bicyclus likely exhibited some degree of plasticity. We propose hypotheses to explain the range of plasticity patterns seen in less seasonal environments and generate testable predictions for the evolution of plasticity in Bicyclus. Our study provides one of the most compelling cases showing links between seasonality and phenotypic plasticity on a macroevolutionary scale and the potential role of plasticity in facilitating the colonization of novel environments.

Staple or delicacy: Sea urchin exploitation over the last 40,000 years at Makpan Cave, Alor Island

Sea urchins are consumed in many parts of the world today. Human consumption of these marine invertebrates can be traced back to at least the Late Pleistocene in various archaeological sites from Island Southeast Asia. Makpan Cave, on Alor Island in Indonesia, is one of the earliest Wallacean prehistoric sites with an occupation record beginning ∼43,000 years ago. Coastal resources (i.e., shellfish, barnacle, crab, and sea urchin) play a dominant role in the subsistence strategy at this site, with urchins important throughout all occupation phases. In this study, we used three different quantification methods (weight, NISP, and MNI) to analyze the over 13 kg of sea urchin remains recovered from Makpan. Our analysis showed that sea urchins were collected during the initial occupation period, when other coastal resources were sparsely utilized. This indicates that sea urchins were intentionally targeted rather than being the result of subsidiary foraging during shellfish collection. The quantity and consistency of sea urchin exploitation at Makpan indicates that urchin was considered a staple food, especially during the initial phase of occupation. We hypothesize that a focus on sea urchins may have been a key strategy for the colonization of novel environments by the earliest human settlers in the region.

Out of the ocean: the timescale of molluscan evolution based on phylogenomics revealed the ages of mollusks’ evolutionary transitions into the novel environment

Being the phylum with the second largest biodiversity, mollusks are widely distributed in marine, freshwater, and land, conquered almost all habitats on the earth. Throughout geological time, several molluscan lineages independently colonized freshwater and land, evolving independently in new habitats. Resolving the timing of their colonization for novel environments is the basis of understanding the complex evolution of Mollusca. Herein, we obtained an elaborate single–copy orthologs set including 107 genes with a total length of 3,447,675 amino acid sites across 134 mollusks to reconstruct the phylogeny of Mollusca. The phylogenetic analysis recovered the “Aculifera+ Conchifera” topology with well–supported. By the divergence times estimation with fossil calibration, we revealed Cambrian rapid diversification of all molluscan classes. What’s more, our results provided the times of three major independent colonization of novel environments and consistent with previous studies. The freshwater mussels (Bivalvia: Unionida) colonized freshwater about 233 Mya, ancient origin and late diversification make this order to become the main represent of the freshwater bivalves. The orders Stylommatophora and Basommatophora (Gastropoda: Pulmonata) respectively colonized land and freshwater about 201 Mya, the Triassic–Jurassic mass extinction may have provided the opportunities for their colonization. Ampullariidae (Gastropoda) colonized freshwater about 156 Mya, their lungs may have contributed to the adaption of tropical freshwater environment and make them survive. Our results probably offer the most comprehensive time–scale of molluscan evolution, could provide some insights into the habitat transition and evolution of Mollusca.

Embryonic and juvenile snakes (Natrix maura, Linnaeus 1758) compensate for high elevation hypoxia via shifts in cardiovascular physiology and metabolism.

The colonization of novel environments requires a favorable response to conditions never, or rarely, encountered in recent evolutionary history. For example, populations colonizing upslope habitats must cope with lower atmospheric pressure at elevation, and thus reduced oxygen availability. The embryo stage in oviparous organisms is particularly susceptible, given its lack of mobility and limited gas exchange via diffusion through the eggshell and membranes. Especially little is known about responses of Lepidosaurian reptiles to reduced oxygen availability. To test the role of physiological plasticity during early development in response to high elevation hypoxia, we performed a transplant experiment with the viperine snake (Natrix maura, Linnaeus 1758). We maintained gravid females originating from low elevation populations (432 m above sea level [ASL]-normoxia) at both the elevation of origin and high elevation (2877 m ASL-extreme high elevation hypoxia; approximately 72% oxygen availability relative to sea level), then incubated egg clutches at both low and high elevation. Regardless of maternal exposure to hypoxia during gestation, embryos incubated at extreme high elevation exhibited altered developmental trajectories of cardiovascular function and metabolism across the incubation period, including a reduction in late-development egg mass. This physiological response may have contributed to the maintenance of similar incubation duration, hatching success, and hatchling body size compared to embryos incubated at low elevation. Nevertheless, after being maintained in hypoxia, juveniles exhibit reduced carbon dioxide production relative to oxygen consumption, suggesting altered energy pathways compared to juveniles maintained in normoxia. These findings highlight the role of physiological plasticity in maintaining rates of survival and fitness-relevant phenotypes in novel environments.

Insect seed and cone predation reduces reproductive potential of treeline conifers across northern Canada

AbstractAimAltitudinal and latitudinal treeline ecotones have not consistently responded to climate warming in the direction and/or magnitude predicted by climate alone, suggesting that non‐climatic mechanisms (e.g. biotic interactions) also mediate treeline range dynamics. Through a collaborative research approach, we assessed environmental conditions associated with pre‐dispersal insect cone granivory and how this biotic interaction may govern the reproductive potential, and therefore range dynamics, of spruce‐dominated treelines across northern Canada.LocationIn all, 10 boreal forest treelines, tundra and alpine, from Yukon to Newfoundland and Labrador, Canada.TaxaWhite spruce (Picea glauca[Moench] Voss), Black spruce (Picea mariana[Mill.] B.S.P.),Strobilomyiaspp.,Megastigmusspp.MethodsTreeline sites were assessed for presence and magnitude of pre‐dispersal seed granivory by insects along with viable seed availability. We quantified stand density metrics, organic layer depth and understorey vegetation composition at each location and, subsequently, incorporated those variables into generalized linear mixed models to establish predictors of granivory magnitude and viability of available seed.ResultsInsect granivory was widespread across sites; however, site‐specific patterns of granivory were associated with increased moss cover and decreased shrub cover and stand density. While all black spruce‐dominated sites exhibited seed viability rates > 50%, the number of seeds produced per cone varied, suggesting that within‐site abiotic conditions and biotic interaction pressures limit successful colonization of novel environments in advance of seed dispersal.Main ConclusionsThe modelled relationships between granivory, seed viability and environmental conditions represent an essential step towards generalizing how and when biotic interactions across subarctic treelines influence boreal tree range dynamics before seed dispersal. Connections between granivory magnitude and site‐level treeline characteristics (e.g. stand density, understorey vegetation) will provide a more comprehensive understanding of treeline range dynamics under continued climate change.

Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands

Phenotypic plasticity enables a single genotype to produce multiple phenotypes in response to environmental variation. Plasticity may play a critical role in the colonization of novel environments, but its role in adaptive evolution is controversial. Here we suggest that rapid parallel regulatory adaptation of Anolis lizards to urban heat islands is due primarily to selection for reduced and/or reversed heat-induced plasticity that is maladaptive in urban thermal conditions. We identify evidence for polygenic selection across genes of the skeletal muscle transcriptome associated with heat tolerance. Forest lizards raised in common garden conditions exhibit heat-induced changes in expression of these genes that largely correlate with decreased heat tolerance, consistent with maladaptive regulatory response to high-temperature environments. In contrast, urban lizards display reduced gene expression plasticity after heat challenge in common garden and a significant increase in gene expression change that is congruent with greater heat tolerance, a putatively adaptive state in warmer urban environments. Genes displaying maladaptive heat-induced plasticity repeatedly show greater genetic divergence between urban and forest habitats than those displaying adaptive plasticity. These results highlight the role of selection against maladaptive regulatory plasticity during rapid adaptive modification of complex systems in the wild.

Adaptation without Specialization Early in a Host Shift.

AbstractStudents of speciation debate the role of performance trade-offs across different environments early in speciation. We tested for early performance trade-offs with a host shift experiment using a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). In this clade of plant-feeding insects, different species live on different host plants and exhibit strong behavioral and physiological host specialization. After five generations, the experimental host shifts resulted either in no adaptation or in adaptation without specialization. The latter result was more likely in sympatry; in allopatry, populations on novel host plants were more likely to become extinct. We conclude that in the early stages of speciation, adaptation to novel host plants does not necessarily bring about performance trade-offs on ancestral environments. Adaptation may be facilitated rather than hindered by gene flow, which prevents extinction. Additional causes of specialization and assortative mating may be required if colonization of novel environments is to result in speciation.

Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

Most ray-finned fishes possess a unique system for retinal oxygen delivery, where intracellular acidification of red blood cells (RBCs) in the retinal capillaries induces oxygen offloading from pH-sensitive hemoglobin. A countercurrent vascular network, the choroid rete mirabile, posterior to the retina augments this “oxygen-secretory” mechanism and confers retinal PO2 values that can exceed 1300 mmHg in some species. We hypothesized that the choroid rete mirabile exerts an active role in intracellular RBC acidification to facilitate retinal oxygen secretion. We show the presence and enzymatic activities of extracellular carbonic anhydrase (CA) and vacuolar-type H+-ATPase (VHA) in the lumen of the choroid rete mirabile. These data are consistent with a pathway, where VHA secretes H+ into the choroid rete mirabile lumen, which combines with HCO3– to form CO2 (catalyzed by extracellular CA) that rapidly diffuses into the RBC facilitating hemoglobin oxygen offloading. Next, we validated the model in vivo by injecting an extracellular CA inhibitor (C18) into the dorsal aorta of anesthetized rainbow trout with a PO2 electrode implanted into the retina. Here, the inhibition of extracellular CA resulted in a rapid reduction in retinal PO2 from 517 to 226 mmHg within minutes. These data strongly support the proposed model for RBC acidification in the choroid rete mirabile. Further, in vivo data show that this mechanism primarily augments oxygen diffusion to the inner retinal segments involved in signal-processing and that the evolution of this pathway was tightly associated with the morphological expansion of this part of the retina. Together, these data suggest that the evolutionary origin of retinal oxygen secretion in the early history of the ray-finned fishes was associated with a greatly enhanced capacity for visual processing, potentially permitting improved visual prey detection and the colonization of novel environments.

Phylogenomics, Biogeography, and Morphometrics Reveal Rapid Phenotypic Evolution in Pythons After Crossing Wallace's Line.

Ecological opportunities can be provided to organisms that cross stringent biogeographic barriers towards environments with new ecological niches. Wallace's and Lyddeker's lines are arguably the most famous biogeographic barriers, separating the Asian and Australo-Papuan biotas. One of the most ecomorphologically diverse groups of reptiles, the pythons, is distributed across these lines, and are remarkably more diverse in phenotype and ecology east of Lydekker's line in Australo-Papua. We used an anchored hybrid enrichment approach, with near complete taxon sampling, to extract mitochondrial genomes and 376 nuclear loci to resolve and date their phylogenetic history. Biogeographic reconstruction demonstrates that they originated in Asia around 38-45 Ma and then invaded Australo-Papua around 23 Ma. Australo-Papuan pythons display a sizeable expansion in morphological space, with shifts towards numerous new adaptive optima in head and body shape, coupled with the evolution of new micro-habitat preferences. We provide an updated taxonomy of pythons and our study also demonstrates how ecological opportunity following colonization of novel environments can promote morphological diversification in a formerly ecomorphologically conservative group. [Adaptive radiation; anchored hybrid enrichment; biogeography; morphometrics; snakes.].

The Epigenetic Signature of Colonizing New Environments in Anolis Lizards

Founder populations often show rapid divergence from source populations after colonizing new environments. Epigenetic modifications can mediate phenotypic responses to environmental change and may be an important mechanism promoting rapid differentiation in founder populations. Whereas many long-term studies have explored the extent to which divergence between source and founder populations is genetically heritable versus plastic, the role of epigenetic processes during colonization remains unclear. To investigate epigenetic modifications in founding populations, we experimentally colonized eight small Caribbean islands with brown anole lizards (Anolis sagrei) from a common source population. We then quantitatively measured genome-wide DNA methylation in liver tissue using reduced representation bisulfite sequencing of individuals transplanted onto islands with high- versus low-habitat quality. We found that lizard sex and habitat quality explained a significant proportion of epigenetic variation. Differentially methylated cytosines mapped to genes that encode proteins with functions likely to be relevant to habitat change (e.g., signal transduction, immune response, circadian rhythm). This study provides experimental evidence of a relationship between epigenetic responses and the earliest stages of colonization of novel environments in nature and suggests that habitat quality influences the nature of these epigenetic modifications.

Evolution: Plasticity versus Selection, or Plasticity and Selection?

Whether phenotypic plasticity enables or hinders genetic adaptation has been debated for over a century. A study of lizard coloration uncovers the means by which plasticity can facilitate colonization of novel environments and enable eventual adaptation by natural selection.

An experimentally introduced population of Brassica rapa (Brassicaceae). 1. Phenotypic selection over three years following colonization of a novel environment

Background and aims – Despite the importance of selection in driving evolution, little is known about the consistency of selection, particularly in the early stages of colonization of novel environments. This study examines the targets and consistency of selection on an experimentally introduced population of the annual plant, Brassica rapa L., in its first three years following introduction to a novel environment. Methods – Phenotypic selection analyses were conducted on a variety of traits collected during the first three years following introduction from California to New York, and the consistency of the strength and direction of selection was examined. Key results – The introduced population experienced direct selection for increased overall size and earlier flowering in 2011 and 2012, and increased height, earlier flowering, and longer duration of flowering in 2013. While the direction of selection only varied for height, inter-annual variation in the strength of selection was observed for a variety of traits, possibly due to changing weather patterns in the introduced environment. Conclusions – The results suggest that selection is dynamic and can fluctuate over time. Thus multi-year assessments of selection are useful for predicting evolutionary responses, particularly in the early stages of colonization of a novel environment.

Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana

Sexual reproduction roots the eukaryotic tree of life, although its loss occurs across diverse taxa. Asexual reproduction and clonal lineages persist in these taxa despite theoretical arguments suggesting that individual clones should be evolutionarily short-lived due to limited phenotypic diversity. Here, we present quantitative evidence that an obligate asexual lineage emerged from a sexual population of the marine diatom Thalassiosira pseudonana and rapidly expanded throughout the world’s oceans. Whole genome comparisons identified two lineages with characteristics expected of sexually reproducing strains in Hardy-Weinberg equilibrium. A third lineage displays genomic signatures for the functional loss of sexual reproduction followed by a recent global colonization by a single ancestral genotype. Extant members of this lineage are genetically differentiated and phenotypically plastic, potentially allowing for rapid adaptation when they are challenged by natural selection. Such mechanisms may be expected to generate new clones within marginal populations of additional unicellular species, facilitating the exploration and colonization of novel environments, aided by exponential growth and ease of dispersal.

Not all weeds are created equal: A database approach uncovers differences in the sexual system of native and introduced weeds.

Weedy species provide excellent opportunities to examine the process of successful colonization of novel environments. Despite the influence of the sexual system on a variety of processes from reproduction to genetic structure, how the sexual system of species influences weediness has received only limited consideration. We examined the hypothesis that weedy plants have an increased likelihood of being self‐compatible compared with nonweedy plants; this hypothesis is derived from Baker's law, which states that species that can reproduce uniparentally are more likely to successfully establish in a new habitat where mates are lacking. We combined a database of the weed (weedy/nonweedy) and introduction status (introduced/native) of plant species found in the USA with a database of plant sexual systems and determined whether native and introduced weeds varied in their sexual systems compared with native and introduced nonweeds. We found that introduced weeds are overrepresented by species with both male and female functions present within a single flower (hermaphrodites) whereas weeds native to the USA are overrepresented by species with male and female flowers present on a single plant (monoecious species). Overall, our results show that Baker's law is supported at the level of the sexual system, thus providing further evidence that uniparental reproduction is an important component of being either a native or introduced weed.

Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats.

Phenotypic plasticity is thought to facilitate the colonization of novel environments and shape the direction of evolution in colonizing populations. However, the relative prevalence of various predicted patterns of changes in phenotypic plasticity following colonization remains unclear. Here, we use a whole-transcriptome approach to characterize patterns of gene expression plasticity in the gills of a freshwater-adapted and a saltwater-adapted ecotype of threespine stickleback (Gasterosteus aculeatus) exposed to a range of salinities. The response of the gill transcriptome to environmental salinity had a large shared component common to both ecotypes (2159 genes) with significant enrichment of genes involved in transmembrane ion transport and the restructuring of the gill epithelium. This transcriptional response to freshwater acclimation is induced at salinities below two parts per thousand. There was also differentiation in gene expression patterns between ecotypes (2515 genes), particularly in processes important for changes in the gill structure and permeability. Only 508 genes that differed between ecotypes also responded to salinity and no specific processes were enriched among this gene set, and an even smaller number (87 genes) showed evidence of changes in the extent of the response to salinity acclimation between ecotypes. No pattern of relative expression dominated among these genes, suggesting that neither gains nor losses of plasticity dominated the changes in expression patterns between the ecotypes. These data demonstrate that multiple patterns of changes in gene expression plasticity can occur following colonization of novel habitats.

Ecological Release from Aquatic Predation Is Associated with the Emergence of Marine Blenny Fishes onto Land.

An ecological release from competition or predation is a frequent adaptive explanation for the colonization of novel environments, but empirical data are limited. On the island of Rarotonga, several blenny fish species appear to be in the process of colonizing land. Anecdotal observations have implied that aquatic predation is an important factor in prompting such amphibious fish behavior. We provide evidence supporting this hypothesis by demonstrating that amphibious blennies shift their abundance up and down the shoreline to remain above predatory fishes that periodically move into intertidal areas during high tide. A predation experiment using blenny mimics confirmed a high risk of aquatic predation for blennies, significantly higher than predation experienced on land. These data suggest that predation has played an active role in promoting terrestrial activity in amphibious blennies and provide a rare example of how ecological release from predation could drive the colonization of a novel environment.

Ecological diversification associated with the benthic‐to‐pelagic transition by North American minnows

Ecological opportunity is often regarded as a key factor that explains why diversity is unevenly distributed across life. Colonization of novel environments or adaptive zones may promote diversification. North American minnows exhibit an ancestral benthic-to-pelagic habitat shift that coincided with a burst in diversification. Here, we evaluate the phenotypic and ecological implications of this habitat shift by assessing craniofacial and dietary traits among 34 species and testing for morphology-diet covariation, convergence and adaptive optima. There were several instances of morphology-diet covariation such as correlations between mouth angle and the consumption of terrestrial insects and between relative gut length and the consumption of algae. After accounting for size and phylogenetic nonindependence, benthic species had longer heads, longer snouts, eyes positioned higher on their head, smaller mouth angles and longer digestive tracts than pelagic minnows. Benthic minnows also consumed more algae but less terrestrial insects, by volume, than pelagic minnows. Lastly, there were three distinct evolutionary regimes and more convergence in morphology and dietary characteristics than expected under a Brownian motion model of evolution. These findings indicate that colonization of the pelagic zone by minnows involved myriad phenotypic and dietary changes associated with exploitation of terrestrial subsidies. Thus, minnows exhibit phenotype-dietary covariation, an expansion of ecological roles and a burst in diversification rates in response to the ecological opportunity afforded by the colonization of a novel habitat.

Receptors rather than signals change in expression in four physiological regulatory networks during evolutionary divergence in threespine stickleback.

The molecular mechanisms underlying behavioural evolution following colonization of novel environments are largely unknown. Molecules that interact to control equilibrium within an organism form physiological regulatory networks. It is essential to determine whether particular components of physiological regulatory networks evolve or if the network as a whole is affected in populations diverging in behavioural responses, as this may affect the nature, amplitude and number of impacted traits. We studied the regulation of four physiological regulatory networks in freshwater and marine populations of threespine stickleback raised in a common environment, which were previously characterized as showing evolutionary divergence in behaviour and stress reactivity. We measured nineteen components of these networks (ligands and receptors) using mRNA and monoamine levels in the brain, pituitary and interrenal gland, as well as hormone levels. Freshwater fish showed higher expression in the brain of adrenergic (adrb2a), serotonergic (htr2a) and dopaminergic (DRD2) receptors, but lower expression of the htr2b receptor. Freshwater fish also showed higher expression of the mc2r receptor of the glucocorticoid axis in the interrenals. Collectively, our results suggest that the inheritance of the regulation of these networks may be implicated in the evolution of behaviour and stress reactivity in association with population divergence. Our results also suggest that evolutionary change in freshwater threespine stickleback may be more associated with the expression of specific receptors rather than with global changes of all the measured constituents of the physiological regulatory networks.

Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments.

We know little about on how frequently transitions into new habitats occur, especially the colonization of novel environments that are the most likely to instigate adaptive evolution. One of the most extreme ecological transitions has been the shift in habitat associated with the move from water to land by amphibious fish. We provide the first phylogenetic investigation of these transitions for living fish. Thirty-three families have species reported to be amphibious and these are likely independent evolutionary origins of fish emerging onto land. Phylogenetic reconstructions of closely related taxa within one of these families, the Blenniidae, inferred as many as seven convergences on a highly amphibious lifestyle. Taken together, there appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families. The colonization of novel habitats by other taxa resulting in less dramatic changes in environment should be equally, if not, more frequent in nature, providing an important prerequisite for subsequent adaptive differentiation.

Successful Colonization of a Novel Urban Environment is Associated with an Urban Behavioural Syndrome in a Reed‐Nesting Waterbird

AbstractUrbanization is currently considered one of the most rapid types of global environmental change. More and more wildlife species are subject to increasing anthropogenic disturbance, but only some of them adapt to become successful urban exploiters. Although a number of fixed life history characteristics may enhance population persistence in an urbanized landscape, behavioural traits are thought to be critical for colonization of a novel urban environment. Within the class of birds, behavioural responses to urban environment have been assessed mostly for passerine species. Here, I examined behavioural alterations in a recently founded urban population of a reed‐nesting rallid species, the Eurasian coot Fulica atra. I found that urban coots adapted to nest in anthropogenically transformed littoral zones with scarce or no emergent vegetation, which precluded efficient nest concealment. Despite this, urban individuals spent, on average, less time incubating due to more frequent bouts off the nest than suburban conspecifics. This pattern was likely possible due to the relaxation of predation pressure in the colonized urban environment. Urban birds were also more aggressive, approached a human intruder at the nest more closely and were more likely to actively defend their nests. Finally, they had a reduced level of physiological stress (as measured with heterophil/lymphocyte ratio) when compared with suburban individuals. In conclusion, the behaviour of coots from the recently founded urban population was consistent with behavioural syndromes found in typical urban exploiters. The results support the central role of behavioural adaptation in successful colonization of novel environments by wildlife.