Environmental temperature serves a major driver for adaptive changes in wild organisms, however, its role in domestication has been less characterized. To uncover the mechanisms of cold tolerance in domestic animals, we sequenced genomes of 28 cattle at median coverage from warm and cold areas across China. By characterizing the population structure and demographic history, we identified two genetic clusters, i.e., northern and southern cattle groups, and a common historic population peak at 30 kilo years ago. Genome scan of cold tolerant breeds revealed genes that under selection sweeps enriched in thermogenesis related pathways. Specifically, we determined a substitution of PRDM16 (p.P779L) in north cattle, which maintains the formation of brown adipocytes through boosting expression of thermogenic related genes, indicating a vital role of this gene in cold tolerance. The findings provide a basis of genetic variations in domestic cattle that shaped by temperature environments and highlight a role of reverse mutation in livestock species.
Organisms exposed to endocrine disruptors in early life can show altered phenotype later in adulthood. Although the mechanisms underlying these long-term effects remain poorly understood, an increasing body of evidence points toward the potential role of epigenetic processes. In the present study, we exposed hatchlings of an isogenic lineage of the self-fertilizing fish mangrove rivulus for 28 days to 4 and 120 ng/L of 17-α-ethinylestradiol. After a recovery period of 140 days, reduced representation bisulfite sequencing (RRBS) was performed on the liver in order to assess the hepatic genome-wide methylation landscape. Across all treatment comparisons, a total of 146 differentially methylated fragments (DMFs) were reported, mostly for the group exposed to 4 ng/L, suggesting a non-monotonic effect of EE2 exposure. Gene ontology analysis revealed networks involved in lipid metabolism, cellular processes, connective tissue function, molecular transport and inflammation. The highest effect was reported for nipped-B-like protein B (NIPBL) promoter region after exposure to 4 ng/L EE2 (+ 21.9%), suggesting that NIPBL could be an important regulator for long-term effects of EE2. Our results also suggest a significant role of DNA methylation in intergenic regions and potentially in transposable elements. These results support the ability of early exposure to endocrine disruptors of inducing epigenetic alterations during adulthood, providing plausible mechanistic explanations for long-term phenotypic alteration. Additionally, this work demonstrates the usefulness of isogenic lineages of the self-fertilizing mangrove rivulus to better understand the biological significance of long-term alterations of DNA methylation by diminishing the confounding factor of genetic variability.
Biomonitoring of complex heterogeneous environments is highly challenging. Fish in deep water bodies occupy different habitats, therefore a combination of survey methods has traditionally been used. Environmental DNA (eDNA) metabarcoding is a novel monitoring tool that can overcome spatial heterogeneity in a highly sensitive and entirely non-invasive manner. However, taxon detection probability is dependent on real-time environmental variables. In this study, three reservoirs were sampled in two seasons using a spatiotemporally distributed sampling design covering major environmental gradients. In all sampling campaigns, 31 fish taxa were detected which exceeded expectations. Data reliability was confirmed by a tight positive correlation between individual taxon scores derived from gillnet sampling and eDNA site occupancy. Analyses confirmed anticipated trends, such as the highest number of taxa were observed in the largest water body, and more taxa were detected in inflows and littoral regions compared to open water. The most important factors for fish distribution were temperature, age and trophic status (expressed as total Chlorophyll a concentration) of water bodies. Taxon detection reflected ecological niches of individual species, e.g. warm water wels catfish (Silurus glanis) and cold water salmonids. This study provides further evidence that eDNA metabarcoding is suitable for ecological study in heterogeneous environments and may substitute conventional fish sampling techniques.
Both aquatic and terrestrial biodiversity information can be detected in riverine water environmental DNA (eDNA). However, the monitoring effectiveness (i.e., the proportion of aquatic and terrestrial biodiversity information detected in riverine water eDNA samples) is unknown. To investigate the monitoring effectiveness, we introduced the concept of watershed biological information flow (WBIF) and proposed that the monitoring effectiveness depended on the transportation effectiveness of the WBIF. Then, the monitoring effectiveness could be assessed in the WBIF framework. Here, we conducted a monitoring effectiveness assessment case study in a watershed on the Qinghai-Tibet Plateau according to analysis of the bacterial operational taxonomic unit (OTU) assemblages detected in riverine water eDNA samples and riparian soil eDNA samples during three seasons. The results showed that (1) the downstream-to-upstream monitoring effectiveness: only 76% of the bacterial OTUs could be detected 1 km downstream in spring and more than 97% and 96% could be detected in summer and autumn, respectively. (2) The river-to-land monitoring effectiveness: more than 62% of the bacterial OTUs in riparian soil eDNA samples could be detected in adjacent riverine water eDNA samples on rainy summer days and 16% and 48% could be detected on cloudy spring and autumn days, respectively. These results suggested that riverine water eDNA was viable for simultaneously monitoring aquatic and terrestrial bacterial biodiversity and that rainy days in summer or autumn were suitable sampling times on the Qinghai-Tibet Plateau. More studies on monitoring effectiveness in other taxonomies and in other watersheds with different climatic conditions are needed.
The mountains of southern China are an excellent system for investigating the processes driving the geographic distribution of biodiversity and radiation of plant populations in response to Pleistocene climate fluctuations. How the key mountain ranges in southern China have affected the evolution of narrowly distributed species is less studied than more widespread species. Here we focused on Cercis chuniana, a woody species endemic to the southern mountain ranges in subtropical China, to elucidate its population dynamics. We used genotyping by sequencing (GBS) to investigate the spatial pattern of genetic variation among 11 populations. Bayesian time estimation revealed that population divergence occurred in the middle Pleistocene, when populations in the Nanling Mts. separated from those to the east. Geographical isolation was detected between the populations located in adjacent mountain ranges, thought to function as geographical barriers due to their complex physiography. As inferred by ecological niche modeling and coalescent simulations, secondary contact occurred during the warm Lushan-Tali interglacial period in China, with intensified East Asia summer monsoon and continuous habitat available for occupation. Complex physiography plus long-term stable ecological conditions across glacial cycles facilitated the demographic expansion in the Nanling Mts., from which contemporary migration began. Our work shows that population genomic approaches are effective in detecting the population dynamics of narrowly distributed species. This study advances our understanding how glacial cycles have affected the evolutionary history of plant species in southern China montane ecosystems.
Intestine regeneration in the sea cucumber Apostichopus japonicus is a fascinating biological event and a typical example for studying host-intestinal microbiota interactions. The intestinal microbiota may play important roles in developing intestine promotion, but the underlying mechanism remains unclear. Notably, altered microbiota abundance may be a key marker of the observed ecosystem. To understand the role of the developing intestinal microbiota in intestine regeneration via quantitative data, we developed a germ-free sea cucumber model and analyzed the intestinal microbial differentiation of faster and slower regenerating A. japonicus individuals during intestine regeneration. The results revealed that depletion of the intestinal microbiota resulted in elevated abundance of the potential key players Flavobacteriaceae and Rhodobacterales during intestine regeneration and thus promoted the intestine regeneration rate of A. japonicus. These results first revealed a direct link between intestinal microbial quantity and microbiome features and the intestinal regrowth rate of A. japonicus. Metagenomic analysis revealed that the increased abundance of Flavobacteriaceae elevated the enrichment of genes associated with carbohydrate utilization, whereas the abundant Rhodobacteraceae -enriched genes were associated with polyhydroxybutyrate production. We identified microbiota abundance as a key driver of microbial community alterations, especially beneficial microbiota members, in the developing intestine of A. japonicus. This study provides new insights into the mechanism of host-microbiota interactions related to intestine development, and the understanding of molecular diversity to questions within intestinal ecology.
Invasive species are of increasing concern to the local biodiversity and ecology as the magnitude of biological invasions is increasing globally. The genetic structures of newly established invasive populations may reveal insights towards the invasion processes, making population genetics an important tool for understanding current invasions. Here we study newly established populations (<10-20 years before first sampling) of the cosmopolitan alien ascidian Botryllus schlosseri in four Puget Sound (Washington, USA) marinas, using eight polymorphic microsatellites. Up to seven sampling sessions over a period of 19 years revealed populations with fluctuating allelic richness (AR=2.693-4.417) and gene diversity (He=0.362-0.589). The populations were well differentiated on spatial and temporal scales and subjected to moderate genetic drift (Fs’=0.027-0.071). The obtained significant heterozygote deficiencies, positive inbreeding coefficients (Fis) and population structure measures (Fst) revealed that no population was under the Hardy-Weinberg equilibrium. Comparing these parameters with those from two Californian sites (Moss Landing and Santa Cruz, 1200 km southerly; invaded by Botryllus during 1940’s) revealed a connection between Moss Landing and Puget Sound, while Santa Cruz remained isolated. On the US west coast scale, this study revealed no major difference in invasive population dynamics between recently and decade long established populations, except for fewer alleles and lower He. When comparing ten worldwide sites, only few microsatellite loci displayed strong regional differences. With globally the lowest numbers of alleles and lowest genetic indices, the Puget Sound Botryllus populations exhibit genetic characteristics of recently established populations, further emerging as one of the youngest B. schlosseri populations, worldwide.
Suitable habitat fragment size, isolation, and distance from a source are important variables influencing community composition of plants and animals, but the role of these environmental factors in determining composition and variation of host-associated microbial communities is poorly known. In parasite-associated microbial communities, it is hypothesized that evolution and ecology of an arthropod parasite will influence its microbiome more than broader environmental factors, but this hypothesis has not been extensively tested. To examine the influence of the broader environment on the parasite microbiome, we applied high-throughput sequencing of the V4 region of 16S rRNA to characterize the microbiome of 222 obligate ectoparasitic bat flies (Streblidae and Nycteribiidae) collected from 155 bats (representing six species) from ten habitat fragments in the Atlantic Forest of Brazil. Parasite species identity is the strongest driver of microbiome composition. To a lesser extent, reduction in habitat fragment area, but not isolation, is associated with an increase in connectance and betweenness centrality of bacterial association networks driven by changes in the diversity of the parasite community. Controlling for the parasite community, bacterial network topology covaries with habitat patch area and exhibits parasite-species specific responses to environmental change. Taken together, habitat loss may have cascading consequences for communities of interacting macro- and microorgansims.
The whitefly Bemisia tabaci is a closely related group of > 35 cryptic species that feed on the phloem sap of a broad range of host plants. Species in the complex differ in their host-range breadth, but the mechanisms involved remain poorly understood. We investigated, therefore, how six different B. tabaci species cope with the environmental unpredictability presented by a set of four common and novel host plants. Behavioural studies indicated large differences in performances on the four hosts and putative specialization of one of the species to cassava plants. Transcriptomic analyses revealed two main insights. First, a large set of genes involved in metabolism (> 85%) showed differences in expression between the six species, and each species could be characterized by its own unique expression pattern of metabolic genes. However, within species, these genes were constitutively expressed, with a low level of environmental responsiveness (i.e., to host change). Second, within each species, sets of genes mainly associated with the super-pathways “environmental information processing” and “organismal systems”, responded to the host switching events. These included genes encoding for proteins involved in sugar homeostasis, signal transduction, membrane transport and immune, endocrine, sensory and digestive responses. Our findings suggested that the six B. tabaci species can be divided into four performance/transcriptomic “Types” and that polyphagy can be achieved in multiple ways. However, polyphagy level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species (the species’ individual metabolic “tool kit”).
Flying fox (Pteropus hypomelanus) belongs to the frugivorous bats, which play a crucial role in maintaining proper functioning of an ecosystem and conservation of environment. Bats are well known carriers of pathogenic viruses such as BatCov RaTG13 from the coronavirus family that share 90.55% with SARS-CoV-2, the pathogen causing recent global pandemic coronavirus disease 19 (COVID-19). However, bats’ possible role as a carrier of pathogenic bacteria is less explored. Here, using metagenomic analysis through high-throughput sequencing, we explored the gut microbiome composition of different island populations on the east and west coasts of Peninsula Malaysia. The 16S rRNA gene in samples from Redang Island, Langkawi Island, Pangkor Island and Tinggi Island was amplified. Bacterial community composition and structure were analyzed with α and β diversity metrics. In contrast to recent studies of host-microbe associations in other mammals, we found no correlation between host phylogeny and bacterial community dissimilarity across four island populations. Our analyses suggest that the significant linear relationship between Redang Island and Langkawi Island implies high bacteria diversity which supporting latitudinal correlation. We found geographic locality is a strong predictor of microbial community composition and observed a positive correlation between ecological features and bacterial richness.
Whilst climate change is recognised as a major future threat to biodiversity, most species are currently threatened by extensive human-induced habitat loss, fragmentation and degradation. Tropical high altitude alpine and montane forest ecosystems and their biodiversity are particularly sensitive to temperature increases under climate change, but they are also subject to accelerated pressures from land conversion and degradation due to a growing human population. We studied the combined effects of anthropogenic land-use change, past and future climate changes and mountain range isolation on the endemic Ethiopian Highlands long-eared bat, Plecotus balensis, an understudied bat that is restricted to the remnant natural high altitude Afroalpine and Afromontane habitats. We integrated ecological niche modelling, landscape genetics and model-based inference to assess the genetic, geographic and demographic impacts of past and recent environmental changes. We show that mountain range isolation and historic climates shaped population structure and patterns of genetic variation, but recent anthropogenic land-use change and habitat degradation are associated with a severe population decline and loss of genetic diversity. Models predict that the suitable niche of this bat has been progressively shrinking since the last glaciation period. This study highlights threats to Afroalpine and Afromontane biodiversity, squeezed to higher altitudes under climate change while losing genetic diversity and suffering population declines due to anthropogenic land-use change. We conclude that the conservation of tropical montane biodiversity requires a holistic approach, using genetic, ecological and geographic information to understand the effects of environmental changes across temporal scales and simultaneously addressing the impacts of multiple threats.
Population and conservation genetics seek to understand how adaptive diversity is shaped by the interweaving forces of molecular evolution in small and endangered populations. On the one hand, selection shapes variation, on the other hand, genetic drift impedes the selection by stochastic changes of allele frequencies. Drift is hypothesised to prevail if the population size is small. However, in practice empirical estimates of the population size are often challenging. Here we used island size as a proxy to population size to reveal the evolutionary constraints of molecular diversity in Toll-like receptors (TLRs) of mockingbirds (genus Mimus) inhabiting Galápagos islands. TLRs are crucial for pathogen recognition by host immunity and thus under various selection constraints. We focused on the interaction of drift and selection in TLR1B, TLR4, and TLR15 across 12 size-variable insular populations and compared them with the mainland population of the northern mockingbird (Mimus polyglottos), aiming to test if population size impacts selection efficiency. Nucleotide diversity positively correlated with the island size indicating an increasing effect of genetic drift in small populations. Despite this pattern, functional TLR properties were largely conserved, presumably due to purifying selection opposing drift independently on the island size. The degree of protein conservatism differed between the loci with TLR15 being the least conserved. Island colonisation did not lead to relaxed selection or to local adaptations. Together with the invariable physicochemical properties of the TLR variants, these observations imply that drift did not outweigh purifying selection despite restricted population size.
Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, particularly regarding highly vulnerable marine ecosystems. Although a large effort has been made to design Marine Protected Areas (MPAs) worldwide, it is still unclear how many species actually exist in these MPAs, what is the genetic connectivity between areas with different protective regimes, and what is their relative genetic diversity. We answer these questions using morphologically cryptic species of the genus Mugil that are sympatric in the largest MPA in the Tropical Southwestern marine province. Population structure analyses show the existence of five highly divergent species (FST > 0.855) and no genetic divergence between two estuaries with different protection status (FST = 0.005). Sympatric individuals are assigned to single clusters and show strong concordance among hundreds of independent gene trees, consistent with full reproductive isolation and no ancestral nor ongoing hybridization. Differences of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions during the evolutionary history of these species, rather than recent impact of fisheries. Together, our results suggest that designing MPAs with areas of integral protection in between areas where fisheries are permitted could be an effective way to manage cryptic species that cannot have species-specific quotas. More generally, this work shows a cost-efficient approach that is transferable to other marine or terrestrial organisms of special concern, helping to implement science-based regulations for management and conservation.
Non-indigenous Daphnia ‘pulex’ have been found in many lakes in New Zealand (NZ) in the past 20 years, suggesting a recent invasion. However, very little is known about the origin of invasive D. ‘pulex’, whether they are D. pulex or D. pulicaria, and whether they are obligately asexual clones or cyclical parthenogens. Furthermore, the source and time of arrival of the invasive genotype(s) are unclear. We address these questions by genomic sequencing Daphnia populations from 13 lakes on the South Island and one on the North Island, NZ. Based on ~24,000 monomorphic species-specific markers, the invasive Daphnia on the South Island were found to be D. pulicaria, while those on the North Island are D. pulex/ pulicaria hybrids. Both the South and North Island Daphnia are phylogenetically clustered with North American D. pulicaria/pulex, thereby suggesting their North American origins. We further found that the South Island Daphnia populations are fixed heterozygotes for nearly all bi-allelic sites in the nuclear genome and contain identical mitochondrial genomes, suggesting the origin and proliferation from a single founder clone, which we experimentally verified to be an obligate asexual. Estimates from molecular data imply a colonization time for the South Island populations of ~ 60 years ago, with a likely invasion route associated with the introduction of salmonids from North America. Key words： Daphnia pulex; Daphnia pulicaria; invasion; obligately asexual; hybridization
Hybridization between species is likely to be associated with a new ecological impact. However, in termites, reports of hybridization mostly focus on hybrid zones caused by species invasion or the development of initial-stage colonies. In this study, we combined microsatellite genotyping with mitochondrial DNA sequencing to investigate the hybridization and adaptive introgression between two sympatric, long-differentiated related termite species, Reticulitermes flaviceps and R. chinensis, in nature. Similar levels of mitochondrial and nuclear genetic diversity were found in R. flaviceps and R. chinensis. Asymmetric interspecific genetic differentiation was observed between mitochondrial and nuclear genes, with high genetic divergence found in mitochondrial DNA but low genetic divergence in nuclear genes. Our results indicated a lack of mitochondrial gene exchange in R. flaviceps and R. chinensis but unconstrained nuclear introgression between them. This asymmetric genetic differentiation between nuclear and cytoplasmic material strongly suggests that there is interspecific hybridization between R. flaviceps and R. chinensis in nature, which provides new insight into the dynamics of hybridization and its potential consequences for speciation in termites.
Tiny predators, especially like phytoseiid mites, often experience a host of threats or stresses by fluctuating environmental factors. Heat acclimation as a superior adaptation strategy critically enhances abilities for organisms to handle with changing climate, but little is known about the molecular mechanism determining tolerant plastic responses in Phytoseiid mites. The relative expression of four identified HSP70 genes in two strains of Neoseiulus barkeri increased within a short time in temperature ramping treatment; meanwhile the expression of NbHSP70-1 and NbHSP70-2 in the conventional strain (CS) sharply decreased after 4 h displaying distinct contrast with the stable expression in the high-temperature adapted strain (HTAS). Western blot analysis showed that the protein level of NbHSP70-1 in CS was dramatically elevated at 0.5 h and decreased at 6 h at 42°C. Conversely, in HTAS, NbHSP70-1 was constantly induced and peaked at 6 h changed at 42°C. Furthermore, HSP70 suppression by RNAi knockdown had a greater influence on the survival of HTAS, causing a higher mortality under high temperature than CS. The recombinant certain exogenous NbHSP70-1 protein enhanced the viability of E. coli BL21 under lethal temperature of 50°C. These results suggested that HSP70 genes were a prominent contributor promoting the thermotolerance to heat stress and plastic change of HSP70 genes conferred the thermotolerance of HTAS through long-term heat acclimation. The divergent constitutive regulation of HSP70 to thermal is conducive to the flexible adaptability of predators in higher trophic level to trade off under extremely adversity stress.
Sexual dimorphism of plumage color is common in avians. A well-known example is mallard, in which drakes exhibit green head feathers, while females exhibit dull head feather color. Through microscopy observations, melanin was observed to be continuously deposited in feather barbules and to form a two-dimensional hexagonal lattice, which conferred the green feather coloration of drakes. Additionally, transcriptome analysis revealed that most pigmentation genes were highly expressed in feather follicles during the development of green feathers, which may contribute to melanin deposition. We identified 18 consensus differentially expressed genes in feather follicles by comparing the transcriptome differences in the male head vs. female head, male head vs. male back, and male head in the 7th week vs. male head in the 11th week. Among these genes, TYRP1 located on Z-chromosome of the mallard genome, showed an increasing trend in the feather follicles of drake heads during green feather development. In particular, its expression was 256 and 32 times higher in the head follicles of males than in those of the female head and the male back, respectively. Hence, the green feathers were determined by TYRP1 through sex-biased expression, which is common for genes linked with Z-chromosome in avians. The differential expression of TYRP1 in different body parts of males and among different time points may be due to differences in cis-regulation by transcription factors. We also demonstrated that the beautiful feather color of other male avians is largely caused by the sex-biased expression of pigmentation genes linked with Z-chromosome.
The symbiotic bacteria associated with honeybee gut have likely transformed from a free-living or parasitic lifestyle, through a close evolutionary association with the insect host. However, little is known about the genomic mechanism underlying bacterial transition to exclusive adaptation to the bee gut. Here we compared the genomes of bee gut symbionts Apibacter with their close relatives living in different lifestyles. We found that despite of general reduction in the Apibacter genome, genes involved in amino acid synthesis and monosaccharide detoxification were retained, which was likely beneficial to the host. Interestingly, the microaerobic Apibacter species have specifically preserved the NAR operon encoding for the nitrate respiration pathway which in contrast, is absent from the related non-free-living microaerobic pathogenic relatives. The NAR operon is also conserved in the cohabiting bee microbe Snodgrasella, but with a differed structure. This convergence implies a crucial role of respiration nitrate reduction for microaerophilic microbiomes to colonize bee gut epithelium. Genes involved in lipid, histidine and phenylacetate degradation are partially lost in Apibacter, possibly associated with the loss of pathogenicity. Antibiotic resistance genes were only sporadically distributed among Apibacter species, but condensed in their pathogenic relatives. Collectively, this study advanced our understanding of genomic transition underlying specialization in bee gut symbionts.