Identification of the maternal source of young‐of‐the‐year Arctic charr in Lake Hazen,Canada

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Genetic divergence between sympatric Arctic charr Salvelinus alpinus morphs in Gander Lake,Newfoundland: roles of migration,mutation and unequal effective population sizes

A suite of 10 microsatellite loci was used to examine genetic divergence between two sympatric morphs of Arctic charr Salvelinus alpinus (‘dark’ and ‘pale’) inhabiting Gander Lake, Newfoundland. Results can be summarized as follows: (1) the morphs are strongly reproductively isolated – gene flow–migration estimates were consistently low in long and short‐term evolutionary timescales of analysis; (2) intermorph divergence based on allele size (R_ST) was significantly larger than those based on allele state (θ) implying a cumulative effect of stepwise‐like mutations; (3) historical (coalescent) and current (linkage disequilibrium) point estimates of effective population size (N_e) were consistently higher for dark than for pale S. alpinus. The first and second findings lend support to the hypothesis that divergence between forms may have preceded the last glacial period (ending c. 12 000 years bp ). The third finding argues for significant differences in habitat quantity and quality between morphs, which were emphasized in a previous study. Overall, these analyses underscore the importance of genetic assessment and monitoring in the conservation of fish diversity, with emphasis on ‘rare’ or under‐represented forms among temperate species pairs.     

Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr

The sub-arctic Lake Fjellfrøsvatn, northern Norway, has two morphs of Arctic charr that are reproductively isolated because they spawn 5 months apart. The smaller morph (≤14 cm L_F ) is confined to the profundal zone of the lake and the larger morph is mainly littoral. Three hypotheses were tested: (i) the offspring of the profundal Arctic charr grow slower than the offspring of the littoral Arctic charr under identical conditions, thus indicating a genetic basis for the slow growth of the profundal Arctic charr in the wild; (ii) the wild phenotypes of the two morphs are morphometrically different and the differences are persistent in the offspring; (iii) the offspring of the two morphs have different behaviour traits under similar treatments. The first hypothesis was rejected; offspring of the profundal morph grew slightly better than offspring of the littoral morph at 10° C in the laboratory. The second and third hypotheses were supported by the data. Wild-caught fish of the two morphs differed in several morphometric characters and most of the differences persisted in the offspring. In the laboratory, offspring of the littoral morph were more active, more aggressive and more pelagic than offspring of the profundal morph and naive offspring of the profundal morph were more effective in eating live chironomid larvae than were offspring of the littoral morph. The data for morphometry and behaviour, but not growth, provide evidence for genetic differences between the two Arctic charr morphs of Fjellfrøsvatn.     

Genetic differences between two sympatric morphs of Arctic charr confirmed by microsatellite DNA

Significant genetic differences ( F _ST = 0·032) were found between littoral and profundal morphs of Arctic charr Salvelinus alpinus from Fjellfrøsvatn, northern Norway, using microsatellite DNA analysis. The morphs had strong reproductive isolation in time and space; the segregation of a separate profundal morph is rare in postglacial lakes.     

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology and migratory behaviour, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole‐genome pooled sequencing of 262 individuals from five taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked whether these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g. areas of low recombination). Consequently, studies employing genome scans to search for areas important for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation.     

Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra

Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such speciation, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macrogyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation‐related hypotheses that differed in the degree of genetic divergence between the morphs. The queen morphs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical amova , 39% of the genetic variation was explained by the queen morph (standardized F'_CT = 0.63, uncorrected F_CT = 0.39), whereas 18% was explained by the locality (F'_SC = 0.39, F_SC = 0.29). This result corroborated the hypothesis of advanced sympatric speciation. In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgynous parasite has genetically diverged from its macrogynous host to the level of a nascent species.     

Speciation and genetic divergence of three species of charr from ancient Lake El'gygytgyn (Chukotka) and their phylogenetic relationships with other representatives of the genus Salvelinus

The diversity of phenotypically different and often reproductively isolated lacustrine forms of charrs of the genus Salvelinus represents a substantial problem for taxonomists and evolutionary biologists. Based on the analysis of variability of ten microsatellite loci and two fragments of mitochondrial DNA (control region and cyt‐b gene), the evolutionary history of three charr species from Lake El'gygytgyn was reconstructed, and phylogenetic relationships between the main representatives of the genus were revealed. Three species from Lake El'gygytgyn were strongly reproductively isolated. Long‐finned charr described previously as Salvethymus svetovidovi, an ancient endemic form in the lake, originated 3.5 Mya (95% Bayesian credible intervals: 1.7, 6.1). Placement of this species in the phylogenetic tree of Salvelinus was not determined strictly, but it should be located in the basal part of the clade Salvelinus alpinus – S. malma species complex. The origin of small‐mouth charr S. elgyticus and Boganida charr S. boganidae in Lake El'gygytgyn was related to allopatric speciation. Their ancestors were represented by two glacial lineages of Taranets charr S. alpinus taranetzi from Asia. In Lake El'gygytgyn, these lineages entered into secondary contact postglacially. A revision of the main phylogenetic groups within the Salvelinus alpinus – S. malma complex is conducted. The Boganida charrs from Lakes El'gygytgyn and Lama (Taimyr) belong to different phylogenetic groups of Arctic charr and should not be regarded as a single species S. boganidae. Using the charrs from Lakes El'gygytgyn and Lama as a case study, we show that a model of sympatric speciation, which seemed more probable based on previous empirical evidence, was rejected by other data.     

Environmental factors associated with genetic and phenotypic divergence among sympatric populations of Arctic charr (Salvelinus alpinus)

The mechanisms by which phenotypic and genetic divergence may occur among sympatric, conspecific populations have been widely discussed but are still not well understood. Possible mechanisms include assortative mating based on morphology or variation in the reproductive behaviour of phenotypes, and both have been suggested to be relevant to the differentiation of salmonid populations in post-glacial lakes. Here, we studied Arctic charr (Salvelinus alpinus) in Windermere, where putative populations are defined by spatial and temporal variation in spawning. Genetic differentiation was assessed based on nine microsatellite loci, and phenotypic variation was assessed from morphometric characters. We test hypotheses about the relative role of morphology, spawning season and spawning habitat in the evolution of genetic divergence among these populations. Distinct from other lake systems, we find that both morphological and genetic differentiation are restricted primarily to one of two interconnecting basins, that genetic and morphological differentiation are decoupled in this lake and that both phenotype and environment have changed over the last 20 years. The implication is that breeding habitat plays a primary role in isolating populations that differentiate by drift and that phenotypically plastic changes, potentially related to foraging specializations, have either become secondarily decoupled from the genetically defined populations or were never fundamental in driving the evolution of genetic diversity in the Windermere system.     

Stocking activities for the Arctic charr in Lake Geneva: Genetic effects in space and time

Artificial stocking practices are widely used by resource managers worldwide, in order to sustain fish populations exploited by both recreational and commercial activities, but their benefits are controversial. Former practices involved exotic strains, although current programs rather consider artificial breeding of local fishes (supportive breeding). Understanding the complex genetic effects of these management strategies is an important challenge with economic and conservation implications, especially in the context of population declines. In this study, we focus on the declining Arctic charr (Salvelinus alpinus) population from Lake Geneva (Switzerland and France), which has initially been restocked with allochtonous fishes in the early eighties, followed by supportive breeding. In this context, we conducted a genetic survey to document the evolution of the genetic diversity and structure throughout the last 50 years, before and after the initiation of hatchery supplementation, using contemporary and historical samples. We show that the introduction of exotic fishes was associated with a genetic bottleneck in the 1980–1990s, a break of Hardy–Weinberg Equilibrium (HWE), a reduction in genetic diversity, an increase in genetic structure among spawning sites, and a change in their genetic composition. Together with better environmental conditions, three decades of subsequent supportive breeding using local fishes allowed to re‐establish HWE and the initial levels of genetic variation. However, current spawning sites have not fully recovered their original genetic composition and were extensively homogenized across the lake. Our study demonstrates the drastic genetic consequences of different restocking tactics in a comprehensive spatiotemporal framework and suggests that genetic alteration by nonlocal stocking may be partly reversible through supportive breeding. We recommend that conservation‐based programs consider local diversity and implement adequate protocols to limit the genetic homogenization of this Arctic charr population.     

Structural genomic variation leads to genetic differentiation in Lake Tanganyika's sardines

Identifying patterns in genetic structure and the genetic basis of ecological adaptation is a core goal of evolutionary biology and can inform the management and conservation of species that are vulnerable to population declines exacerbated by climate change. We used reduced‐representation genomic sequencing methods to gain a better understanding of genetic structure among and within populations of Lake Tanganyika's two sardine species, Limnothrissa miodon and Stolothrissa tanganicae. Samples of these ecologically and economically important species were collected across the length of Lake Tanganyika, as well as from nearby Lake Kivu, where L. miodon was introduced in 1959. Our results reveal differentiation within both S. tanganicae and L. miodon that is not explained by geography. Instead, this genetic differentiation is due to the presence of large sex‐specific regions in the genomes of both species, but involving different polymorphic sites in each species. Our results therefore indicate rapidly evolving XY sex determination in the two species. Additionally, we found evidence of a large chromosomal rearrangement in L. miodon, creating two homokaryotypes and one heterokaryotype. We found all karyotypes throughout Lake Tanganyika, but the frequencies vary along a north–south gradient and differ substantially in the introduced Lake Kivu population. We do not find evidence for significant isolation by distance, even over the hundreds of kilometres covered by our sampling, but we do find shallow population structure.     

Low levels of hybridization between sympatric Arctic char (Salvelinus alpinus) and Dolly Varden char (Salvelinus malma) highlights their genetic distinctiveness and ecological segregation

Understanding the extent of interspecific hybridization and how ecological segregation may influence hybridization requires comprehensively sampling different habitats over a range of life history stages. Arctic char (Salvelinus alpinus) and Dolly Varden (S. malma) are recently diverged salmonid fishes that come into contact in several areas of the North Pacific where they occasionally hybridize. To better quantify the degree of hybridization and ecological segregation between these taxa, we sampled over 700 fish from multiple lake (littoral and profundal) and stream sites in two large, interconnected southwestern Alaskan lakes. Individuals were genotyped at 12 microsatellite markers, and genetic admixture (Q) values generated through Bayesian‐based clustering revealed hybridization levels generally lower than reported in a previous study (<0.6% to 5% of samples classified as late‐generation hybrids). Dolly Varden and Arctic char tended to make different use of stream habitats with the latter apparently abandoning streams for lake habitats after 2–3 years of age. Our results support the distinct biological species status of Dolly Varden and Arctic char and suggest that ecological segregation may be an important factor limiting opportunities for hybridization and/or the ecological performance of hybrid char.     

Balancing sample accumulation and DNA degradation rates to optimize noninvasive genetic sampling of sympatric carnivores

Noninvasive genetic sampling, or noninvasive DNA sampling (NDS), can be an effective monitoring approach for elusive, wide‐ranging species at low densities. However, few studies have attempted to maximize sampling efficiency. We present a model for combining sample accumulation and DNA degradation to identify the most efficient (i.e. minimal cost per successful sample) NDS temporal design for capture–recapture analyses. We use scat accumulation and faecal DNA degradation rates for two sympatric carnivores, kit fox (Vulpes macrotis) and coyote (Canis latrans) across two seasons (summer and winter) in Utah, USA, to demonstrate implementation of this approach. We estimated scat accumulation rates by clearing and surveying transects for scats. We evaluated mitochondrial (mtDNA) and nuclear (nDNA) DNA amplification success for faecal DNA samples under natural field conditions for 20 fresh scats/species/season from <1–112 days. Mean accumulation rates were nearly three times greater for coyotes (0.076 scats/km/day) than foxes (0.029 scats/km/day) across seasons. Across species and seasons, mtDNA amplification success was ≥95% through day 21. Fox nDNA amplification success was ≥70% through day 21 across seasons. Coyote nDNA success was ≥70% through day 21 in winter, but declined to <50% by day 7 in summer. We identified a common temporal sampling frame of approximately 14 days that allowed species to be monitored simultaneously, further reducing time, survey effort and costs. Our results suggest that when conducting repeated surveys for capture–recapture analyses, overall cost‐efficiency for NDS may be improved with a temporal design that balances field and laboratory costs along with deposition and degradation rates.     

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum‐likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host‐associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall‐forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host‐plant‐associated differentiation were greater in the non‐gall‐inducing parasites than in their gall‐inducing hosts. RNA‐seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host‐plant relationships. Our results suggest a mode of speciation in which host plants drive within‐guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.     

Population genetic structure and adaptive differentiation of iron walnut Juglans regia subsp. sigillata in southwestern China

Southwestern (SW) China is an area of active tectonism and erosion, yielding a dynamic, deeply eroded landscape that influences the genetic structure of the resident populations of plants and animals. Iron walnut (Juglans regia subsp. sigillata) is a deciduous tree species endemic to this region of China and cultivated there for its edible nuts. We sampled 36 iron walnut populations from locations throughout the species' range in SW China and genotyped a total of 765 individuals at five chloroplast DNA regions and 22 nuclear microsatellite loci. Species distribution models were produced to predict the evolution and historical biogeography of iron walnut and to estimate the impacts of climate oscillations and orographic environments on the species' demography. Our results indicated that J. regia subsp. sigillata had relatively low genetic diversity, high interpopulation genetic differentiation, and asymmetric interpopulation gene flow. Based on DIYABC analysis, we identified two lineages of J. sigillata in southwestern China. The lineages (subpopulations) diverge during the last glacial period (~1.34 Ma). Southwestern China was a glacial refuge during the last glacial period, but increasingly colder and arid climates might have fostered the fragmentation of J. regia subsp. sigillata within this refugium. Finally, we found that recent habitat fragmentation has led to a reduction in population connectivity and increased genetic differentiation by genetic drift in isolated populations. Our results support a conclusion that geological and climatic factors since the Miocene triggered the differentiation, evolutionary origin, and range shifts of J. sigillata in the studied region.     

Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot‐specific NADPH oxidase

Root hairs are instrumental for nutrient uptake in monocot cereals. The maize (Zea mays L.) roothairless5 (rth5) mutant displays defects in root hair initiation and elongation manifested by a reduced density and length of root hairs. Map‐based cloning revealed that the rth5 gene encodes a monocot‐specific NADPH oxidase. RNA‐Seq, in situ hybridization and qRT‐PCR experiments demonstrated that the rth5 gene displays preferential expression in root hairs but also accumulates to low levels in other tissues. Immunolocalization detected RTH5 proteins in the epidermis of the elongation and differentiation zone of primary roots. Because superoxide and hydrogen peroxide levels are reduced in the tips of growing rth5 mutant root hairs as compared with wild‐type, and Reactive oxygen species (ROS) is known to be involved in tip growth, we hypothesize that the RTH5 protein is responsible for establishing the high levels of ROS in the tips of growing root hairs required for elongation. Consistent with this hypothesis, a comparative RNA‐Seq analysis of 6‐day‐old rth5 versus wild‐type primary roots revealed significant over‐representation of only two gene ontology (GO) classes related to the biological functions (i.e. oxidation/reduction and carbohydrate metabolism) among 893 differentially expressed genes (FDR <5%). Within these two classes the subgroups ‘response to oxidative stress’ and ‘cellulose biosynthesis’ were most prominently represented.     

Maternal genetic effects on adaptive divergence between anadromous and resident brook charr during early life history

The importance of directional selection relative to neutral evolution may be determined by comparing quantitative genetic variation in phenotype (Q(ST)) to variation at neutral molecular markers (F(ST)). Quantitative divergence between salmonid life history types is often considerable, but ontogenetic changes in the significance of major sources of genetic variance during post-hatch development suggest that selective differentiation varies by developmental stage. In this study, we tested the hypothesis that maternal genetic differentiation between anadromous and resident brook charr (Salvelinus fontinalis Mitchill) populations for early quantitative traits (embryonic size/growth, survival, egg number and developmental time) would be greater than neutral genetic differentiation, but that the maternal genetic basis for differentiation would be higher for pre-resorption traits than post-resorption traits. Quantitative genetic divergence between anadromous (seawater migratory) and resident Laval River (Québec) brook charr based on maternal genetic variance was high (Q(ST) > 0.4) for embryonic length, yolk sac volume, embryonic growth rate and time to first response to feeding relative to neutral genetic differentiation [F(ST) = 0.153 (0.071-0.214)], with anadromous females having positive genetic coefficients for all of the above characters. However, Q(ST) was essentially zero for all traits post-resorption of the yolk sac. Our results indicate that the observed divergence between resident and anadromous brook charr has been driven by directional selection, and may therefore be adaptive. Moreover, they provide among the first evidence that the relative importance of selective differentiation may be highly context-specific, and varies by genetic contributions to phenotype by parental sex at specific points in offspring ontogeny. This in turn suggests that interpretations of Q(ST)-F(ST) comparisons may be improved by considering the structure of quantitative genetic architecture by age category and the sex of the parent used in estimation.