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The three-spined stickleback (Gasterosteus aculeatus) has repeatedly and independently adapted to freshwater habitats from standing genetic variation (SGV) following colonization from the sea. However, in the Mediterranean Sea G. aculeatus is believed to have gone extinct, and thus the spread of locally adapted alleles between different freshwater populations via the sea since then has been highly unlikely. This is expected to limit parallel evolution, that is the extent to which phylogenetically related alleles can be shared among independently colonized freshwater populations. Using whole genome and 2b-RAD sequencing data, we compared levels of genetic differentiation and genetic parallelism of 15 Adriatic stickleback populations to 19 Pacific, Atlantic and Caspian populations, where gene flow between freshwater populations across extant marine populations is still possible. Our findings support previous studies suggesting that Adriatic populations are highly differentiated (average F-ST approximate to 0.45), of low genetic diversity and connectivity, and likely to stem from multiple independent colonizations during the Pleistocene. Linkage disequilibrium network analyses in combination with linear mixed models nevertheless revealed several parallel marine-freshwater differentiated genomic regions, although still not to the extent observed elsewhere in the world. We hypothesize that current levels of genetic parallelism in the Adriatic lineages are a relic of freshwater adaptation from SGV prior to the extinction of marine sticklebacks in the Mediterranean that has persisted despite substantial genetic drift experienced by the Adriatic stickleback isolates.

Parallel evolution of similar morphologies in closely related lineages provides insight into the repeatability and predictability of evolution. In the genus Antirrhinum (snapdragons), as in other plants, a suite of morphological characters are associated with adaptation to alpine environments.We test for parallel trait evolution in Antirrhinum by investigating phylogenetic relationships using Restriction-site associated DNA (RAD) sequencing. We then associate phenotypic information to our phylogeny to reconstruct patterns of morphological evolution and relate this to evidence for hybridization between emergent lineages.Phylogenetic analyses show that the alpine character syndrome is present in multiple groups, suggesting that Antirrhinum has repeatedly colonised alpine habitats. Dispersal to novel environments happened in the presence of intraspecific and interspecific gene flow.We find support for a model of parallel evolution in Antirrhinum. Hybridisation in natural populations, and a complex genetic architecture underlying the alpine morphology syndrome, support an important role of natural selection in maintaining species divergence in the face of gene flow.

Biologists have long been intrigued by apparently predictable and repetitive evolutionary trajectories inferred across a variety of lineages and systems. In recent years, high-throughput sequencing analyses have started to transform our understanding of such repetitive shifts. While researchers have traditionally categorized such shifts as either "convergent" or "parallel," based on relatedness of the lineages involved, emerging genomic insights provide an opportunity to better describe the actual evolutionary mechanisms at play. A synthesis of recent genomic analyses confirms that convergence is the predominant driver of repetitive evolution among species, whereas repeated sorting of standing variation is the major driver of repeated shifts within species. However, emerging data reveal numerous notable exceptions to these expectations, with recent examples of de novo mutations underpinning convergent shifts among even very closely related lineages, while repetitive sorting processes have occurred among even deeply divergent taxa, sometimes via introgression. A number of very recent analyses have found evidence for both processes occurring on different scales within taxa. We suggest that the relative importance of convergent versus sorting processes depends on the interplay between gene flow among populations, and phylogenetic relatedness of the lineages involved.

Organisms use color for camouflage, sexual signaling, or as a warning sign of danger. Primates are one of the most vibrantly colored Orders of mammals. However, the genetics underlying their coat color are poorly known, limiting our ability to study molecular aspects of its evolution. The role of the melanocortin 1 receptor (MC1R) in color evolution has been implicated in studies on rocket pocket mice (Chaetodipus intermediusi), toucans (Ramphastidae), and many domesticated animals. From these studies, we know that changes in MC1R result in a yellow/red or a brown/black morphology. Here, we investigate the evolution of MC1R in Lorisidae, a monophyletic nocturnal primate family, with some genera displaying high contrast variation in color patterns and other genera being monochromatic. Even more unique, the Lorisidae family has the only venomous primate: the slow loris (Nycticebus). Research has suggested that the contrasting coat patterns of slow lorises are aposematic signals for their venom. If so, we predict the MC1R in slow lorises will be under positive selection. In our study, we found that Lorisidae MC1R is under purifying selection (ω = 0.0912). In Lorisidae MC1R, there were a total of 75 variable nucleotides, 18 of which were nonsynonymous. Six of these nonsynonymous substitutions were found on the Perodicticus branch, which our reconstructions found to be the only member of Lorisidae that has predominantly lighter coat color; no substitutions were associated with Nycticebus. Our findings generate new insight into the genetics of pelage color and evolution among a unique group of nocturnal mammals and suggest putative underpinnings of monochromatic color evolution in the Perodicticus lineage., In primates, the most colorful of mammals, few have examined the influence the melanocortin 1 receptor (MC1R) has on color variation (light or dark) in primates. Here, we examined how MC1R impacts color variation in a cryptic primate family with high contrasting color variation. We found MC1R is under purifying selection, but there appears to be a link in nucleotide changes and light coat color.

Parallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing to track seasonal allele frequency changes in six of these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

The evolution of resistance has been seen across all major classes of xenobiotics, including antimicrobial drugs and agricultural pesticides. This repeated emergence of resistance is a case of phenotypic parallel evolution, but often the parallelism extends to the molecular level too, with multiple species gaining the same mutation in response to the same chemical treatment. We review the degree of repeatability in target‐site resistance mutations affecting different classes of site‐specific agricultural fungicides used in crop protection, comparing the extent to which resistance in different pathogen species has evolved via the same or different mutations. For all major fungicide target sites, substantial levels of molecular parallel evolution can be seen, with at least one mutation recurring in over 50% of species. Target‐site mutations appear to be most repeatable in cytochrome b, target site of quinone‐outside inhibitor fungicides, and least predictable for CYP51, target site of the azoles. Intermediate levels of repeatability are seen for the MBC target site β‐tubulin, and the SDHI target site succinate dehydrogenase. Repeatability may be lower where there are selective trade‐offs between resistance and pleiotropic fitness penalties, or differing levels of cross‐resistance across members of a fungicide class; or where single mutations confer only partial resistance, and epistatic interactions between multiple mutations result in a rugged fitness landscape. This affects the predictive power of in vitro mutation studies, and has practical implications for resistance monitoring strategies and diagnostic methods.

Habitats can select for specialized phenotypic characteristics in animals. However, the consistency of evolutionary responses to particular environmental conditions remains difficult to predict. One trait of great ecological importance is brain form, which is expected to vary between habitats that differ in their cognitive requirements. Here, we compared divergence in brain form and oral jaw size across a common littoral-pelagic ecological axis in two sunfishes at both the intraspecific and interspecific levels. Brain form differed between habitats at every level of comparison; however, divergence was inconsistent, despite consistent differences in oral jaw size. Pumpkinseed and bluegill species differed in cerebellum, optic tectum and olfactory bulb size. These differences are consistent with a historical ecological divergence because they did not manifest between littoral and pelagic ecotypes within either species, suggesting constraints on changes to these regions over short evolutionary time scales. There were also differences in brain form between conspecific ecotypes, but they were inconsistent between species. Littoral pumpkinseed had larger brains than their pelagic counterpart, and littoral bluegill had smaller telencephalons than their pelagic counterpart. Inconsistent brain form divergence between conspecific ecotypes of pumpkinseed and bluegill sharing a common littoral-pelagic habitat axis suggests that contemporary ecological conditions and historic evolutionary context interact to influence evolutionary changes in brain form in fishes.

Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

Parallel evolution is one of the striking patterns in nature. The presence of repeated evolution of the same phenotypes, suites of traits, and adaptations suggests a strong role for natural selection in shaping biological diversity. The reasoning is straightforward: each instance of repeated evolution makes it less likely that these features evolved neutrally or due to stochastic forces in each population or species. With the growing sequencing capability, we are now poised to examine the genetic basis of parallel evolution in model and nonmodel systems. On pages 4102-4117 of this issue of Molecular Ecology, van Boheemen and Hodgins (2020) provide an exemplar study of this kind, using common ragweed (Ambrosia artemisiifolia; Figure 1a). Their study is noteworthy and ambitious in many respects, and we think will serve as a model for studying parallel adaptation, even in nonmodel species.

[Aim] One of the main goals of functional biogeography is to examine distribution patterns of trait diversity, and islands provide excellent study cases for this emerging field. We tested the hypothesis that multiple dispersals from a common mainland pool would promote functional similarity among island systems when environmental conditions are similar, but also novel phenotypic traits related to colonization history and exploitation of new habitats., [Location] Mediterranean Basin and Macaronesian islands., [Taxon] Wolfbane (Periploca laevigata), [Methods] We used the well‐known biogeographical history of a woody plant complex (P. laevigata s.l.) to examine trait variation and how it relates to climatic conditions of mainland and subtropical island settings. In a common garden experiment, we measured a suite of leaf physiological and anatomical traits tightly related to plant performance in 320 seedlings representing 21 populations of five sublineages—the oldest (2.6 my) island colonization (western Canary Islands) as a reference, three sublineages stemming from independent events of island colonization in the last 0.5 my from NW Africa (Cape Verde, Fuerteventura, Lanzarote) and their widespread Mediterranean mainland counterpart., [Results] We observed strong phenotypic divergence between island and mainland sublineages linked to contrasting climatic conditions. Mediterranean mainland populations displayed a very specialized leaf phenotype characteristic of arid plants (i.e. small leaves, amphistomaty, isobilateral mesophyll, high photosynthetic rates). In turn, low seasonality on islands was linked to the recurrent expression of a phenotype characterized by larger leaves and lower photosynthetic rates. Our analyses showed that the high investment in secondary compounds (i.e. tannins) on islands decouples photosynthesis from growth rates. Despite this pattern of parallel differentiation, each island sublineage displayed a distinctive phenotype, with some traits related to colonization time, which resulted in a mosaic of functional variation across island systems., [Main conclusions] Our data suggest that the studied subtropical islands promote expression of traits specific to certain sublineages and other common traits that are no longer adaptive in the original mainland pool due to Pleistocene climatic shifts. These findings ultimately extend the role of islands as biodiversity refugia and hotspots of plant functional diversity., This research was funded by the European Regional Development Fund (Intereg projects CAVEGEN and ENCLAVES). C. G‐V was financially supported by a ‘Vicenç Mut' postdoctoral fellowship (Conselleria d'Innovació, Recerca i Turisme, Govern de les Illes Balears and the European Social Fund).

Complete loss of petals, or becoming apetalous, has occurred independently in many flowering plant lineages. However, the mechanisms underlying the parallel evolution of naturally occurring apetalous lineages remain largely unclear. Here, by sampling representatives of all nine apetalous genera/tribes of the family Ranunculaceae and conducting detailed morphological, expression, molecular evolutionary and functional studies, we investigate the mechanisms underlying parallel petal losses. We found that while non-expression/downregulation of the petal identity gene APETALA3-3 (AP3-3) is tightly associated with complete petal losses, disruptions of the AP3-3 orthologs were unlikely to be the real causes for the parallel evolution of apetalous lineages. We also found that, compared with their close petalous relatives, naturally occurring apetalous taxa usually bear slightly larger numbers of stamens, whereas the number of sepals remains largely unchanged, suggestive of petal-to-stamen rather than petal-to-sepal transformations. In addition, in the recently originated apetalous genus Enemion, the petal-to-stamen transformations have likely been caused by the mutations that led to the elevation and outward expansion of the expression of the C-function gene, AGAMOUS1 (AG1). Our results not only provide a general picture of parallel petal losses within the Ranunculaceae but also help understand the mechanisms underlying the independent originations of other apetalous lineages.

Predicting speciation is a fundamental goal of research in evolutionary ecology. The probability of speciation is often positively correlated with ecosystem size. Although the mechanisms driving this correlation are generally difficult to identify, a shared geographical and ecological context provides a suitable condition to study the mechanisms that promote speciation in large ecosystems by reducing the number of factors to be considered. Here, we determined the correlation between speciation and ecosystem size, and discuss the underlying mechanisms of this relationship, using a probable parallel ecotype formation for freshwater fish. Our population genetic analysis revealed that speciation of the landlocked goby, Rhinogobius sp. YB, of the Ryukyu Archipelago, Japan, from its migratory ancestor, R. brunneus, occurred in parallel across five islands. Logistic regression analysis showed that speciation probability could be predicted using island size. The results suggest that ecosystem size predicts the occurrence of adaptation and reproductive isolation, probably through its association with three possible factors: divergent selection strength, population persistence, and occurrence probability of habitat separation., 大きな島で種分化が起きやすいことを解明 --「キバラヨシノボリ」は琉球列島で5回誕生した--. 京都大学プレスリリース. 2020-05-13.

Vision represents an excellent model for studying adaptation, given the genotype-to-phenotype-map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we characterized the visual system of Neotropical Characiformes, which is the result of several spectral tuning mechanisms acting in concert including gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2-chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform’s entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS- and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. In addition, characiforms exhibited species-specific differences in opsin expression. Finally, we found interspecific and intraspecific variation in the use of A1/A2-chromophores correlating with the light environment. These multiple mechanisms may be a result of the highly diverse visual environments where Characiformes have evolved.

Cities are emerging as models for addressing the fundamental question of whether populations evolve in parallel to similar environments. Here, we examine the environmental factors that drive parallel evolutionary urban-rural clines in a Mendelian trait — the cyanogenic antiherbivore defense of white clover (Trifolium repens). We sampled over 700 urban and rural clover populations across 16 cities along a latitudinal transect in eastern North America. In each population, we quantified the frequency of genotypes that produce hydrogen cyanide (HCN), and in a subset of the cities we estimated the frequency of the alleles at the two genes (CYP79D15 and Li) that epistatically interact to produce HCN. We then tested the hypothesis that winter environmental conditions cause the evolution of clines in HCN by comparing the strength of clines among cities located along a gradient of winter temperatures and frost exposure. Overall, half of the cities exhibited urban-rural clines in the frequency of HCN, whereby urban populations evolved lower HCN frequencies. The weakest clines in HCN occurred in cities with the lowest temperatures but greatest snowfall, supporting the hypothesis that snow buffers plants against winter frost and constrains the formation of clines. By contrast, the strongest clines occurred in the warmest cities where snow and frost are rare, suggesting that alternative selective agents are maintaining clines in warmer cities. Additionally, some clines were driven by evolution at only CYP79D15, consistent with stronger and more consistent selection on this locus than on Li. Together, our results demonstrate that both the agents and targets of selection vary across cities and highlight urban environments as large-scale models for disentangling the causes of parallel evolution in nature.Impact SummaryUnderstanding whether independent populations evolve in the same way (i.e., in parallel) when subject to similar environments remains an important problem in evolutionary biology. Urban environments are a model for addressing the extent of parallel evolution in nature due to their convergent environments (e.g. heat islands, pollution, fragmentation), such that two distant cities are often more similar to one another than either is to nearby nonurban habitats. In this paper, we used white clover (Trifolium repens) as a model to study the drivers of parallel evolution in response to urbanization. We collected >11,000 plants from urban and rural habitats across 16 cities in eastern North America to examine how cities influence the evolution of a Mendelian polymorphism for an antiherbivore defense trait – hydrogen cyanide (HCN). This trait had previously been shown to exhibit adaptive evolution to winter temperature gradients at continental scales. Here we tested the hypothesis that winter environmental conditions cause changes in the frequency of HCN between urban and rural habitats. We found that half of all cities had lower frequency of HCN producing genotypes relative to rural habitats, demonstrating that cities drive parallel losses of HCN in eastern North America. We then used environmental data to understand why cities vary in the extent to which they drive reduction in HCN frequencies. The warmest cities showed the greatest reductions in HCN frequencies in urban habitats, while colder, snowier cities showed little change in HCN between urban and rural habitats. This suggests that snow weakens the strength of natural selection against HCN in cities. However, it additionally suggests alternative ecological or evolutionary mechanisms drive the strong differences in HCN between urban and rural habitats in the warmest cities. Overall, our work highlights urban environments as powerful, large-scale models for disentangling the causes of parallel and non-parallel evolution in nature.

Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye-expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant-based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and-unusually for echolocating bats-often have large, well-developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar-feeding lineages and the subfamily Stenodermatinae of fig-eating bats fine-tuning pre-existing visual adaptations for specialized purposes.

Our understanding of the evolution of complex biological traits is greatly advanced by examining taxa with intermediate phenotypes. The transition from oviparity (egg-laying) to viviparity (live-bearing) has occurred independently in many animal lineages, but there are few phenotypic intermediates. The lizard Saiphos equalis exhibits bimodal reproduction, with some viviparous populations, and other oviparous populations with long egg-retention, a rare trait where most of embryonic development occurs inside the mother prior to late ovipositioning. We posit that oviparous S. equalis represent an intermediate form between "true" oviparity and viviparity. We used transcriptomics to compare uterine gene expression in these two phenotypes, and provide a molecular model for the genetic control and evolution of reproductive mode. Many genes are differentially expressed throughout the reproductive cycle of both phenotypes, which have clearly different gene expression profiles overall. The differentially expressed genes within oviparous and viviparous individuals have broadly similar biological functions putatively important for sustaining embryos, including uterine remodelling, respiratory gas and water exchange, and immune regulation. These functional similarities indicate either that long egg-retention is an exaptation for viviparity, or might reflect parallel evolution of similar gravidity-related changes in gene expression in long egg-retention oviparity. In contrast, gene expression changes across the reproductive cycle of long egg-retaining oviparous S. equalis are dramatically different from those of "true" oviparous skinks (such as Lampropholis guichenoti), supporting our assertion that oviparous S. equalis exhibit an intermediate phenotype between "true" oviparity and viviparity.

Premise Despite intensive research, the pathways and driving forces behind the evolution of derived woodiness on oceanic islands remain obscure. The genus Daucus comprises mostly herbs (therophytes, hemicryptophytes) with few rosette treelets (chamaephytes) endemic to various Macaronesian archipelagos, suggesting their independent evolution. To elucidate the evolutionary pathways to derived woodiness, we examined phylogenetic relationships and the habit and secondary xylem evolution in Daucus and related taxa. Methods Sixty taxa were surveyed for molecular markers, life history, and habit traits. Twenty-one species were considered for wood anatomical characters. A dated phylogeny was estimated using Bayesian methods. The evolution of selected traits was reconstructed using parsimony and maximum likelihood. Results Daucus dispersed independently to the Canary Islands (and subsequently to Madeira), Cape Verde, and the Azores in the late Miocene and Pleistocene. Life span, reproductive strategy, and life form were highly homoplastic; the ancestor of Daucus was probably a monocarpic, biennial hemicryptophyte. Rosette treelets evolved independently in the Canarian-Madeiran lineage and in Cape Verde, the latter within the last 0.13 Myr. Treelets and hemicryptophytes did not differ in wood anatomy. Pervasive axial parenchyma in wood occurred more often in polycarpic rather than monocarpic species. Conclusions Life span and life form in Daucus are evolutionarily labile and may change independently of wood anatomy, which is related to plant reproductive strategy rather than to life form. Insular woodiness may evolve rapidly (as demonstrated in D. bischoffii), and in Daucus, it does not seem to be an adaptation to lower the risk of xylem embolism.

Similar phenotypes evolve under equivalent environmental conditions through parallel evolution. Because they have repeatedly invaded and adapted to new freshwater environments, the three-spined stickleback (Gasterosteus aculeatus) offers a powerful system for understanding the agents of selection in nature that drive parallel evolution. Here we examine the ecological and environmental variables responsible for morphological variation in three-spined stickleback populations across its European range. We collected fish from 85 populations, encompassing much of the European latitudinal range of the species and including lowland rivers and lakes, coastal lagoons, and moorland ponds. We measured biotic and environmental variables at all sites along with morphological traits for 2,358 individuals. Using an information theory approach, we identified body size, minimum average winter temperature and pH as primary predictors of stickleback armour evolution, challenging current hypotheses for stickleback morphological diversification and demonstrating the fundamental role played by body size and scaling in mediating responses to selection. Stickleback lateral plate phenotype represents a potentially powerful tool for monitoring change in climate variables across the northern temperate region.

Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post-glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole-genome sequence data of 41 outcrossing populations, we identified loci associated with three niche-determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage-specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level.

One of the most notable evolutionary innovations of marine invertebrates is the snapping claw of alpheid shrimps (Alpheidae), capable of generating a powerful water jet and a shock wave, used for defense, aggression, excavation, and communication. Evolutionary analysis of this character complex requires the study of a suite of complementary traits to discern pre-adaptations or post-adaptations of snapping behavior. A comprehensive phylogenetic analysis of the Alpheidae based on two mitochondrial and four nuclear markers, covering 107 species from 38 genera (77.6% generic coverage), is presented. Ancestral state reconstruction analyses revealed five independent origins of snapping, two of which relate to the morphologically similar but phylogenetically distant genera Alpheus and Synalpheus, highlighting significant convergence. The evolution of the five complementary traits (adhesive plaques, tooth-cavity system, dactylar joint type, chela size enlargement, and orbital hood) did not always show a significant correlation with the evolution of snapping overall, sometimes only in a few lineages, suggesting different evolutionary pathways were involved and demonstrating the versatility in the evolution of the snapping mechanisms.

Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into sympatric benthic and pelagic ecotypes across multiple independent lakes. We found that genes differentially spliced between ecotypes were mostly not differentially expressed (, see also the Perspective by Sarah J. Salisbury, M. Lisette Delgado and Anne C. Dalziel.

In this issue of Molecular Ecology, Yamasaki et al. (2020) use genetic data from extensive sampling of Rhinogobius goby fish across the Ryukyu Archipelago in Japan to demonstrate the parallel speciation of a freshwater form from an ancestral amphidromous form. They then show that ecosystem size strongly predicts the probability of speciation between the two forms across islands. In doing so, this study connects population-level processes (microevolution) to broad-scale biodiversity patterns (macroevolution), an important but understudied link in evolutionary biology. Moving forward, we can build on this research to (a) more directly determine how geographic, ecological and historical factors influence the different stages of the speciation process, and (b) understand whether mechanisms inferred from insular radiations extend to those on continents, where both demographic histories and environmental regimes are likely more complex.

Hybridization and convergent evolution are phenomena of broad interest in evolutionary biology, but their occurrence poses challenges for reconstructing evolutionary affinities among affected taxa. Sticklebacks in the genus Pungitius are a case in point: evolutionary relationships and taxonomic validity of different species and populations in this circumpolarly distributed species complex remain contentious due to convergent evolution of traits regarded as diagnostic in their taxonomy, and possibly also due to frequent hybridization among taxa. To clarify the evolutionary relationships among different Pungitius species and populations globally, as well as to study the prevalence and extent of introgression among recognized species, genomic data sets of both reference genome-anchored single nucleotide polymorphisms and de novo assembled RAD-tag loci were constructed with RAD-seq data. Both data sets yielded topologically identical and well-supported species trees. Incongruence between nuclear and mitochondrial DNA-based trees was found and suggested possibly frequent hybridization and mitogenome capture during the evolution of Pungitius sticklebacks. Further analyses revealed evidence for frequent nuclear genetic introgression among Pungitius species, although the estimated proportions of autosomal introgression were low. Apart from providing evidence for frequent hybridization, the results challenge earlier mitochondrial and morphology-based hypotheses regarding the number of species and their affinities in this genus: at least seven extant species can be recognized on the basis of genetic data. The results also shed new light on the biogeographical history of the Pungitius-complex, including suggestion of several trans-Arctic invasions of Europe from the Northern Pacific. The well-resolved phylogeny should facilitate the utility of this genus as a model system for future comparative evolutionary studies.

Root system architecture (RSA) is a critical aspect of plant growth and competitive ability. Here we used two independently evolved strains of weedy rice, a de-domesticated form of rice, to study the evolution of weed-associated RSA traits and the extent to which they evolve through shared or different genetic mechanisms. We characterised 98 two-dimensional and three-dimensional RSA traits in 671 plants representing parents and descendants of two recombinant inbred line populations derived from two weed × crop crosses. A random forest machine learning model was used to assess the degree to which root traits can predict genotype and the most diagnostic traits for doing so. We used quantitative trait locus (QTL) mapping to compare genetic architecture between the weed strains. The two weeds were distinguishable from the crop in similar and predictable ways, suggesting independent evolution of a 'weedy' RSA phenotype. Notably, comparative QTL mapping revealed little evidence for shared underlying genetic mechanisms. Our findings suggest that despite the double bottlenecks of domestication and de-domestication, weedy rice nonetheless shows genetic flexibility in the repeated evolution of weedy RSA traits. Whereas the root growth of cultivated rice may facilitate interactions among neighbouring plants, the weedy rice phenotype may minimise below-ground contact as a competitive strategy.

Adaptation often proceeds via the sorting of standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection between populations. Nor is it clear whether the availability of standing variation for adaptation affects progress toward speciation in a manner that depends on the difference in the direction of selection. We conducted a theoretical study investigating these questions and have two primary findings. First, the extent of parallel genetic evolution between two populations is expected to rapidly decline as the difference in their directions of selection increases from fully parallel toward divergent, and this decline occurs more rapidly in organisms with greater trait ‘dimensionality’. This rapid decline results because seemingly small differences in the direction of selection cause steep reductions in the fraction of alleles that are beneficial in both populations. For example, populations adapting to optima separated by an angle of 33° have only 50% of potentially beneficial alleles in common (for a case of five trait ‘dimensions’). Second, we find that adaptation from standing variation leads to higher ecologically-dependent hybrid fitness under parallel selection, relative to when adaptation is from new mutation only. This occurs because genetic parallelism based on standing variation reduces the phenotypic segregation variance in hybrids when parents adapt to similar environments. In contrast, under divergent selection, the pleiotropic effects of alternative alleles fixed from standing variation change the major axes of phenotypic variation in hybrids and reduce their fitness in parental habitats. We conclude that adaptation from standing genetic variation is expected to slow progress toward speciation via parallel natural selection and can facilitate progress toward speciation via divergent natural selection.Impact summaryIt is increasingly clear that much of adaptation, especially that which occurs rapidly, proceeds from the sorting of ancestral standing variation rather than complete reliance onde novomutation. In addition, evolutionary biologists are increasingly embracing the fact that the difference in the direction of natural selection on pairs of populations is a quantitative continuum ranging from completely parallel to completely divergent. In this article, we ask two questions. First, how does the degree of genetic parallelism—here, adaptation using the same alleles in allopatric populations—depend on the differences in the direction of natural selection acting on two populations, from parallel (0°) to divergent (180°)? And second, how does adaptation from standing variation affect progress toward speciation, and does its effect depend on the direction of natural selection? We develop theory to address these questions. We first find that very small differences in the direction of selection (angle) can largely preclude genetic parallelism. Second, we find that adaptation from standing variation has implications for speciation that change along the continuum from parallel to divergent selection. Under parallel selection, high genetic parallelism causes inter-population hybrids to have high mean fitness when their parents adapt from standing variation. As selection tends toward divergent, adaptation from standing variation is less beneficial for hybrid fitness and under completely divergent selection causes inter-population hybrids to have lower mean fitness than when adaptation was from new mutation alone. In sum, our results provide general insight into patterns of genetic parallelism and speciation along the continuum of parallel to divergent natural selection when adaptation is from standing variation.

The evolution of herbicide resistance in crop weeds presents one of the greatest challenges to agriculture and the production of food. Herbicide resistance has been studied for more than 60 yr, in the large part by researchers seeking to design effective weed control programs. As an outcome of this work, various unique questions in plant adaptation have been addressed. Here, I collate recent research on the herbicide-resistant problem in light of key questions and themes in evolution and ecology. I highlight discoveries made on herbicide-resistant weeds in three broad areas - the genetic basis of adaptation, evolutionary constraints, experimental evolution - and similarly discuss questions left to be answered. I then develop how one would use herbicide-resistance evolution as a model for studying eco-evolutionary dynamics within a community context. My overall goals are to highlight important findings in the weed science literature that are relevant to themes in plant adaptation and to stimulate the use of herbicide-resistant plants as models for addressing key questions within ecology and evolution.

Evidence that organisms evolve rapidly enough to alter ecological dynamics necessitates investigation of the reciprocal links between ecology and evolution. Data that link genotype to phenotype to ecology are needed to understand both the process and ecological consequences of rapid evolution. Here, we quantified the suite of elements in individuals (i.e., ionome) and differences in the fluxes of key nutrients across populations of threespine stickleback. We find that allelic variation associated with freshwater adaptation that controls bony plating is associated with changes in the ionome and nutrient recycling. More broadly, we find that adaptation of marine stickleback to freshwater conditions shifts the ionomes of natural populations and populations raised in common gardens. In both cases ionomic divergence between populations was primarily driven by differences in trace elements rather than elements typically associated with bone. These findings demonstrate the utility of ecological stoichiometry and the importance of ionome-wide data in understanding eco-evolutionary dynamics.

Studies of parallel or convergent evolution (the repeated, independent evolution of similar traits in similar habitats) rarely explicitly quantify the extent of parallelism (i.e. variation in the direction and/or magnitude of divergence) between the sexes; instead, they often investigate both sexes together or exclude one sex. However, differences in male and female patterns of divergence could contribute to overall variation in the extent of parallelism among ecotype pairs, especially in sexually dimorphic traits. Failing to properly attribute such variation could lead to underestimates of the importance of environmental variation in shaping phenotypes. We investigate the extent of parallelism in the body shape of male and female beach and creek spawning sockeye salmon (Oncorhynchus nerka) from two lake systems in western Alaska that were colonized independently after the last ice age. Although both sexes showed some degree of parallelism, patterns of beach-creek body shape divergence vary between the sexes and between lake systems. Phenotypic change vector analyses revealed highly parallel aspects of divergence between males from different lake systems (males from beaches had deeper bodies than males from creeks) but weaker parallelism in females and high parallelism between the sexes in one lake system but not the other. Body shape also had population-specific components, which were mostly, but not entirely, explained by environmental variation in the form of creek depth. Our results highlight the importance of explicitly considering the extent of parallelism between the sexes and environmental variation among sites within habitat types.

The independent and repeated adaptation of populations to similar environments often results in the evolution of similar forms. This phenomenon creates a strong correlation between phenotype and environment and is referred to as parallel evolution. However, we are still largely unaware of the dynamics of parallel evolution, as well as the interplay between phenotype and genotype within natural systems. Here, we examined phenotypic and genotypic parallel evolution in multiple parapatric Dune-Headland coastal ecotypes of an Australian wildflower, Senecio lautus. We observed a clear trait-environment association in the system, with all replicate populations having evolved along the same phenotypic evolutionary trajectory. Similar phenotypes have arisen via mutational changes occurring in different genes, although many share the same biological functions. Our results shed light on how replicated adaptation manifests at the phenotypic and genotypic levels within populations, and highlight S. lautus as one of the most striking cases of phenotypic parallel evolution in nature. This work was supported by an Australian Research Council grant (DP190103039) to DO and JE, and a University of Queensland Graduate School International Travel Award to MEJ