Digest: Hybridization as a buffer against thermal extremes.

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve.

In November 2004, the Arctic Council, a coordinating body of the eight Arctic nations (Canada, Denmark, Iceland, Sweden, Nor-way, Finland, Russia, and the United States) released its Arctic Climate Impact Assessment: Impacts of a Warming Arctic (ACIA). Emerging from the work of hundreds of scientists and incorporating indigenous knowledge about conditions in the Arctic, the ACIA paints a sobering picture of the effect of present and expected global warming on Arctic peoples and ecosystems. Although a few Arctic areas have cooled over recent decades, overall average surface air temperatures have risen almost twice as much as global averages. In Alaska and western Canada, temperatures have risen 3–4°C since 1954. For the whole Arctic, the ACIA projects additional warming of 4–7°C over the next century. These projections are not a worst-case scenario; they are based on low-to-middle projections from the United Nations Intergovernmental Panel on Climate Change. The focus of the ACIA was not temperatures, though, but the ecological, cultural, and economic impacts of warming. A few impacts could be positive: marine transportation should improve as ice retreats from shorelines, and vegetation growth may also accelerate in warmer conditions, perhaps increasing food production. But land transportation has already become more difficult due to melting of permafrost; ice highways used to transport industrial and mining equipment are now available for shorter periods each winter. Ice-free oceans, combined with melting permafrost, have already resulted in severe erosion and coastal destruction in Alaska. In terms of ecology, the impacts are largely negative. Over the past few decades, the amount of boreal forest that burned each year has doubled, and the ACIA says forest insect outbreaks and forest fires are “very likely” to intensify. As ice continues to retreat from the Arctic Ocean, animals that live on or hunt under the ice, including polar bears and several seal species, could grow scarcer or even go extinct. Caribou in the giant Porcupine River herd in northwest Canada and Alaska are drowning as they cross rivers that normally are still ice when the animals migrate. Warming has also interfered with caribou feeding, says Craig Fleener, a wildlife biologist for the Gwich’in Council International, an indigenous group for whom the Porcupine River herd provides a material and cultural foundation. Repeated freezing and thawing, he says, creates a very hard, crusty layer on the ground that makes it hard for the caribou to reach the lichen that is their major food source. “What is really happening is rapid climate and environmental change that goes beyond our capability of adapting quickly enough,” says Fleener. “If the change happens over a long period, we can find new methods, a new place to live or harvest, but when you have rapid change, it is much more difficult [to adapt].” Hunters are also being affected more directly, says Sheila Watt-Cloutier, chair of the Inuit Circumpolar Conference, one of six indigenous organizations that contributed to the report. “As a result of warming,” she says, “Inuit hunters are falling through the thinning ice.” Hunting is the basis of Inuit culture, she stresses, and an economic necessity because imported food prices reflect high transportation costs. The Inuit include 155,000 Arctic natives living in eastern Siberia, North America, and Greenland. The report is a wake-up call, says Jonathan Foley, director of the Center for Sustainability and the Global Environment at the University of Wisconsin–Madison, but not just for Arctic residents. Polar snow and ice reflect solar radiation out to space, he points out. As the snow and ice retreat, the Earth’s surface gets darker and absorbs more heat, warming the whole planet in a dangerous feedback loop where warming causes melting and melting causes warming. Watt-Cloutier observes that Arctic peoples already face the threat of high levels of organic pollutants such as dioxin and poly-chlorinated biphenyls that have drifted north through the atmosphere and now contaminate animal fat and human breast milk. With the prospect of greenhouse gases produced further south causing disproportionate warming in the Arctic, the region is once again “being poisoned from afar,” she says. Arctic people are resilient by necessity and tradition, says Watt-Cloutier, and they have come through enormous, sudden, tumultuous change in the last 50–60 years caused by the introduction of culture, technology, and foods from the temperate regions. But the Arctic way of life is wedded to a specific environment, and that environment is rapidly changing. While much of the press coverage of the ACIA report has focused on the possibility that polar bears could become extinct, she warns, “It’s not just about endangered species of animals. We ourselves are an endangered species.”

BackgroundThe parthenogenetic Caucasian rock lizard Darevskia armeniaca, like most other parthenogenetic vertebrate species, originated through interspecific hybridization between the closely related sexual Darevskia mixta and Darevskia valentini. Darevskia armeniaca was shown to consist of one widespread allozyme clone and a few rare ones, but notwithstanding the origin of clonal diversity remains unclear. We conduct genomic analysis of D. armeniaca and its parental sexual species using microsatellite and SNP markers to identify the origin of parthenogenetic clonal lineages.ResultsFour microsatellite-containing loci were genotyped for 111 specimens of D. armeniaca, 17 D. valentini, and four D. mixta. For these species, a total of 47 alleles were isolated and sequenced. Analysis of the data revealed 13 genotypes or presumptive clones in parthenogenetic D. armeniaca, including one widespread clone, two apparently geographically restricted clones, and ten rare clones. Comparisons of genotype-specific markers in D. armeniaca with those of its parental species revealed three founder-events including a common and two rare clones. All other clones appeared to have originated via post-formation microsatellite mutations in the course of evolutionary history of D. armeniaca.ConclusionOur new approach to microsatellite genotyping reveals allele-specific microsatellite and SNP markers for each locus studied. Interspecies comparison of these markers identifies alleles inherited by parthenospecies from parental species, and provides new information on origin and evolution of clonal diversity in D. armeniaca. SNP analyses reveal at least three interspecific origins of D. armeniaca, and microsatellite mutations in these initial clones give rise to new clones. Thus, we first establish multiple origins of D. armeniaca. Our study identifies the most effective molecular markers for elucidating the origins of clonal diversity in other unisexual species that arose via interspecific hybridization.

Hybridogenesis in an interspecific hybrid frog is a coupling mechanism in the gametogenic cell line that eliminates the genome of one parental species with endoduplication of the remaining genome of the other parental species. It has been intensively investigated in the edible frog Pelophylax kl. esculentus (RL), a natural hybrid between the marsh frog P. ridibundus (RR) and the pool frog P. lessonae (LL). However, the genetic mechanisms involved remain unclear. Here, we investigated the water frogs in the western Russian territory. In three of the four populations, we genetically identified 16 RL frogs living sympatrically with the parental LL species, or with both parental species. In addition, two populations contained genome introgression with another species, P. bedriagae (BB) (a close relative of RR). In the gonads of 13 RL frogs, the L genome was eliminated, producing gametes of R (or R combined with the B genome). In sharp contrast, one RL male eliminated the L or R genome, producing both R and L sperm. We detected a variation in genome elimination within a population. Based on the genetic backgrounds of RL frogs, we hypothesize that the introgression of the B genome resulted in the change in choosing a genome to be eliminated.

Interspecific hybridization can lead to myriad outcomes, including transgressive phenotypes in which the hybrids are more fit than either parent species. Such hybrids may display important traits in the context of climate change, able to respond to novel environmental conditions not previously experienced by the parent populations. While this has been evaluated in an agricultural context, the role of transgressive hybrids under changing conditions in the wild remains largely unexplored; this is especially true regarding transgressive gene expression. Using the blue mussel species complex (genus Mytilus) as a model system, we investigated the effects of hybridization on temperature induced gene expression plasticity by comparing expression profiles in parental species and their hybrids following a 2-week thermal challenge. Hybrid expression plasticity was most often like one parent or the other (50%). However, a large fraction of genes (26%) showed transgressive expression plasticity (i.e. the change in gene expression was either greater or lesser than that of both parent species), while only 2% were intermediately plastic in hybrids. Despite their close phylogenetic relationship, there was limited overlap in the differentially expressed genes responding to temperature, indicating interspecific differences in the responses to high temperature in which responses from hybrids are distinct from both parent species. We also identified differentially expressed long non-coding RNAs (lncRNAs), which we suggest may contribute to species-specific differences in thermal tolerance. Our findings provide important insight into the impact of hybridization on gene expression under warming. We propose transgressive hybrids may play an important role in population persistence under future warming conditions.

Hybrid performance and species crossability relationships in willows (<i>Salix</i>)

The twenty-first century is likely to be characterised by large changes in regional climatic and environmental conditions, with implications for the availability and distribution of key resources such as water and productive land. While the implications of such changes for human societies are potentially profound, the empirical evidence base for understanding human–environment interactions focuses largely on the relatively recent past, during which examples of rapid and severe climate change are lacking. While there are no precise past analogues for twenty-first century climate change, the Middle Holocene Climatic Transition (MHCT), from about 6400–5000 years before present, provides us with an example of a period of large-scale global climatic reorganisation, punctuated by episodes of rapid and severe climate change, at a time when human societies were beginning to resemble those of today. A survey of archaeological and palaeo-environmental data from the northern hemisphere subtropics and other regions provides us with evidence for linked climatic, environmental and societal change during the MHCT. This evidence, the strength of which varies with location, allows us to construct convincing narratives of linked climatic, environmental and societal changes that accommodate a variety of responses and outcomes, and that are much more nuanced than narratives of the proposed climate-induced collapse of individual societies. Such synthetic studies that compare contexts across time and space can help us understand human–environment interactions during times of climatic disruption, while allowing for diverse outcomes and avoiding the pitfalls of climatic determinism.

Genomic introgression through interspecific hybridization has been observed in some species of the freshwater fish family Cobitidae. Within this family, a Cobitis hankugensis–Iksookimia longicorpa diploid–triploid hybrid species complex on the Korean peninsula is unique in displaying hybridogenesis, a unisexual reproduction mode that allows hybrids to mediate the transfer of mitochondrial DNA (but not nuclear DNA) between the two parent species. However, populations of the parental species in the wild have never been examined for the potential effect of introgression on their genomes. To address the genetic consequences of unisexual hybridization on the parental species, we examined genetic structure of the two parental species, C. hankugensis and I. longicorpa, in three independent natural habitats where they coexist with their hybrid complex using DNA sequence data of one mitochondrial gene and three nuclear genes. We found that mitochondrial introgression between the two species was extensive in all the examined localities, while there was no evidence of nuclear introgression across the species boundary. This result indicates that the hybridogenetic individuals mediate mitochondrial introgression from one species to the other, producing mito‐nuclear mosaic genomes such as C. hankugensis nuclear genomes associated with I. longicorpa mitochondrial DNA and the reverse. The direction and degree of introgression varied among the three localities, but the underlying mechanisms for this observation proved elusive. Introgression might depend on which species serves as the predominant sperm or ovum donor or the environmental conditions of the localities. The present study suggests that introgressive hybridization between pure C. hankugensis and I. longicorpa species is highly likely where the two species co‐occur with hybridogenetic individuals, but the consequence of introgression could be variable due to the history and environmental characteristics of particular populations across the parental species’ ranges.

NOR loci of C-subgenome are dominant in wheat×Aegilops interspecific hybrids, which may have evolutionary implications for wheat group genome dynamics and evolution. After interspecific hybridisation, some genes are often expressed from only one of the progenitor species, shaping subsequent allopolyploid genome evolution processes. A well-known example is nucleolar dominance, i.e. the formation of cell nucleoli from chromosomes of only one parental species. We studied nucleolar organizing regions (NORs) in diploid Aegilops markgrafii (syn: Ae. caudata; CC), Ae. umbellulata (UU), allotetraploids Aegilops cylindrica (CcCcDcDc) and Ae. triuncialis (CtCtUtUt), synthetic interspecific F1 hybrids between these two allotetraploids and bread wheat (Triticum aestivum, AABBDD) and in F3 generation hybrids with genome composition AABBDDCtCtUtUt using silver staining and fluorescence in situ hybridization (FISH). In Ae. markgrafii (CC), NORs of both 1C and 5C or only 5C chromosome pairs were active in different individual cells, while only NORs on 1U chromosomes were active in Ae. umbellulata (UU). Although all 35S rDNA loci of the Ct subgenome (located on 1Ct and 5Ct) were active in Ae. triuncialis, only one pair (occupying either 1Cc or 5Cc) was active in Ae. cylindrica, depending on the genotype studied. These C-genome expression patterns were transmitted to the F1 and F3 generations. Wheat chromosome NOR activity was variable in Ae. triuncialis×T. aestivum F1 seeds, but silenced by the F3 generation. No effect of maternal or paternal cross direction was observed. These results indicate that C-subgenome NOR loci are dominant in wheat×Aegilops interspecific hybrids, which may have evolutionary implications for wheat group genome dynamics and allopolyploid evolution.

Disc electrophoresis of tuber proteins from Solanum species and interspecific hybrids

The Korea Meteorological Agency (KMA) has monitored flowering dates over the past 100 years for seven economically important woody plant species. This unique dataset is perfect for understanding whether historical patterns of phenological plasticity are breaking down in the face of recent and rapid climate change. Here we show that a scientist armed only 50 years into this study would have been able to predict the phenological shifts of the last 50 years with a high degree of accuracy. This is despite record-breaking warm temperatures and unprecedented early flowering, suggesting consistency in phenological shifts over time. Shifts in the timing of spring flowering events are recognized as one of the clearest and most sensitive ecological indicators of climate change 1 . Numerous efforts are under way to track yearly variation in flowering phenology 2,3 , but most ongoing studies began in the last few decades and so lack data on phenology before the onset of anthropogenic climate change. Such studies typically calculate phenological sensitivity as the linear relationship between flowering time and temperature, but there is emerging uncertainty as to whether plants may be reaching the limit of their ability to track temperature 4, 5 . If they are reaching this limit, we would expect to see either non-linearities (e.g., asymptotes) in phenological sensitivity 6 , or increased variability (or a lack of predictability) in comparison with what were once tight, strong relationships 7 . Indeed, some have suggested that drivers such as winter chilling and photoperiod will become more prominent in cueing flowering as spring temperatures become less limiting 8 . To gain an understanding of whether climate change is resulting in different patterns of phenological response, we need to compare recent shifts to historical baseline data from before the onset of rapid anthropogenic climate change. .

The International Union for the Conservation of Nature (IUCN) Red List has led efforts to monitor and conserve populations of animals, plants, and fungi since 1964. However, recent research suggests the list is not effectively accounting for the consequences of rapid man-made climate change. The Korean Water Deer (Hydropotes inermis argyropus) is classified as vulnerable internationally, but in South Korea it is widely considered a pest, with the government offering bounties to cull what are considered high numbers. Both the IUCN’s classification and the Korean government’s approach to Korean Water Deer fail to consider the possibility of a rapid decline in numbers due to rapidly spreading biosecurity threats facilitated by rapid climate change. This paper describes the current status of Korean Water Deer, the biosecurity threats the population faces, and potential solutions to protect the population. This case study of Korean Water Deer will also add to evidence that the IUCN’s classification system is failing to accurately describe the potential for rapid collapse of mammal populations due to biosecurity threats facilitated by climate change.

Tropical forests play a critical role in carbon and water cycles at a global scale. Rapid climate change is anticipated in tropical regions over the coming decades and, under a warmer and drier climate, tropical forests are likely to be net sources of carbon rather than sinks. However, our understanding of tropical forest response and feedback to climate change is very limited. Efforts to model climate change impacts on carbon fluxes in tropical forests have not reached a consensus. Here, we use the Ecosystem Demography model (ED2) to predict carbon fluxes of a Puerto Rican tropical forest under realistic climate change scenarios. We parameterized ED2 with species-specific tree physiological data using the Predictive Ecosystem Analyzer workflow and projected the fate of this ecosystem under five future climate scenarios. The model successfully captured interannual variability in the dynamics of this tropical forest. Model predictions closely followed observed values across a wide range of metrics including aboveground biomass, tree diameter growth, tree size class distributions, and leaf area index. Under a future warming and drying climate scenario, the model predicted reductions in carbon storage and tree growth, together with large shifts in forest community composition and structure. Such rapid changes in climate led the forest to transition from a sink to a source of carbon. Growth respiration and root allocation parameters were responsible for the highest fraction of predictive uncertainty in modeled biomass, highlighting the need to target these processes in future data collection. Our study is the first effort to rely on Bayesian model calibration and synthesis to elucidate the key physiological parameters that drive uncertainty in tropical forests responses to climatic change. We propose a new path forward for model-data synthesis that can substantially reduce uncertainty in our ability to model tropical forest responses to future climate.

The recent publication of the summary for policy makers by Working Group I of the Intergovernmental Panel on Climate Change (IPCC) [1] has injected a renewed sense of urgency to address climate change. It is therefore timely to review the notion of preventing 'dangerous anthropogenic interference with the climate system' as put forward in the United Nations Framework Convention on Climate Change (UNFCCC). The article by Danny Harvey in this issue [2] offers a fresh perspective by rephrasing the concept of 'dangerous interference' as a problem of risk assessment. As Harvey points out, identification of 'dangerous interference' does not require us to know with certainty that future climate change will be dangerous—an impossible task given that our knowledge about future climate change includes uncertainty. Rather, it requires the assertion that interference would lead to a significant probability of dangerous climate change beyond some risk tolerance, and therefore would pose an unacceptable risk.

Strong karotypic orthoselection does not fully account for genome size variation in pines. Adult F1 interspecific pine hybrids are fertile and the genomic consequences of hybridization can be studied using haploid female megagametophytes. Greater variation in genome size was hypothesized to occur in hybrids compared to their parental species and the variation was thought to be positively related to the phylogenetic distance between the parental species. Nuclear 1C DNA content of megagametophytes from four sets of fertile Pinus spp. F1 hybrids and their parents was determined using a laser flow cytometer. Fertile F1 hybrids included two sets of hard pine hybrid Pinus elliottii Engelm. x P. caribaea var. hondurensis Morelet and two Asian x New World soft pine hybrids P. wallichiana A.B. Jacks. x P. strobus L. (hybrid is known as P. x schwerinii) and P. lambertiana Dougl. x P. armandii Franchlet. Fertile, adult F1 produce haploid megagametophytes with nuclear DNA contents comparable to the parents or parental species. One genomic consequence of hybridization in pines is stability in nuclear DNA content. Hybrid genomes neither increased or decreased DNA content regardless of the phylogenetic distance between parents. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 503–508.