Rethinking ecological niches and geographic distributions in face of pervasive human influence in the Anthropocene.

Species are distributed in predictable ways in geographic spaces. The three principal factors that determine geographic distributions of species are biotic interactions (B), abiotic conditions (A), and dispersal ability or mobility (M). A species is expected to be present in areas that are accessible to it and that contain suitable sets of abiotic and biotic conditions for it to persist. A species' probability of presence can be quantified as a combination of responses to B, A, and M via ecological niche modeling (ENM; also frequently referred to as species distribution modeling or SDM). This analytical approach has been used broadly in ecology and biogeography, as well as in conservation planning and decision-making, but commonly in the context of 'natural' settings. However, it is increasingly recognized that human impacts, including changes in climate, land cover, and ecosystem function, greatly influence species' geographic ranges. In this light, historical distinctions between natural and anthropogenic factors have become blurred, and a coupled human-natural landscape is recognized as the new norm. Therefore, B, A, and M (BAM) factors need to be reconsidered to understand and quantify species' distributions in a world with a pervasive signature of human impacts. Here, we present a framework, termed human-influenced BAM (Hi-BAM, for distributional ecology that (i) conceptualizes human impacts in the form of six drivers, and (ii) synthesizes previous studies to show how each driver modifies the natural BAM and species' distributions. Given the importance and prevalence of human impacts on species distributions globally, we also discuss implications of this framework for ENM/SDM methods, and explore strategies by which to incorporate increasing human impacts in the methodology. Human impacts are redefining biogeographic patterns; as such, future studies should incorporate signals of human impacts integrally in modeling and forecasting species' distributions.

Carotenoid sequestration protein FIBRILLIN participates in CmOR-regulated ß-carotene accumulation in melon.

Chromoplasts are plant organelles with a unique ability to sequester and store massive carotenoids. Chromoplasts have been hypothesized to enable high levels of carotenoid accumulation due to enhanced sequestration ability or sequestration substructure formation. However, the regulators that control the substructure component accumulation and substructure formation in chromoplasts remain unknown. In melon (Cucumis melo) fruit, ß-carotene accumulation in chromoplasts is governed by ORANGE (OR), a key regulator for carotenoid accumulation in chromoplasts. By using comparative proteomic analysis of a high ß-carotene melon variety and its isogenic line low-ß mutant that is defective in CmOr with impaired chromoplast formation, we identified carotenoid sequestration protein FIBRILLIN1 (CmFBN1) as differentially expressed. CmFBN1 expresses highly in melon fruit tissue. Overexpression of CmFBN1 in transgenic Arabidopsis (Arabidopsis thaliana) containing ORHis that genetically mimics CmOr significantly enhances carotenoid accumulation, demonstrating its involvement in CmOR-induced carotenoid accumulation. Both in vitro and in vivo evidence showed that CmOR physically interacts with CmFBN1. Such an interaction occurs in plastoglobules and results in promoting CmFBN1 accumulation. CmOR greatly stabilizes CmFBN1, which stimulates plastoglobule proliferation and subsequently carotenoid accumulation in chromoplasts. Our findings show that CmOR directly regulates CmFBN1 protein levels and suggest a fundamental role of CmFBN1 in facilitating plastoglobule proliferation for carotenoid sequestration. This study also reveals an important genetic tool to further enhance OR-induced carotenoid accumulation in chromoplasts in crops.

Pan-genome and multi-parental framework for high-resolution trait dissection in melon (Cucumis melo).

Linking genotype with phenotype is a fundamental goal in biology and requires robust data for both. Recent advances in plant-genome sequencing have expedited comparisons among multiple-related individuals. The abundance of structural genomic within-species variation that has been discovered indicates that a single reference genome cannot represent the complete sequence diversity of a species, leading to the expansion of the pan-genome concept. For high-resolution forward genetics, this unprecedented access to genomic variation should be paralleled and integrated with phenotypic characterization of genetic diversity. We developed a multi-parental framework for trait dissection in melon (Cucumis melo), leveraging a novel pan-genome constructed for this highly variable cucurbit crop. A core subset of 25 diverse founders (MelonCore25), consisting of 24 accessions from the two widely cultivated subspecies of C. melo, encompassing 12 horticultural groups, and 1 feral accession was sequenced using a combination of short- and long-read technologies, and their genomes were assembled de novo. The construction of this melon pan-genome exposed substantial variation in genome size and structure, including detection of ~300 000 structural variants and ~9 million SNPs. A half-diallel derived set of 300 F2 populations, representing all possible MelonCore25 parental combinations, was constructed as a framework for trait dissection through integration with the pan-genome. We demonstrate the potential of this unified framework for genetic analysis of various melon traits, including rind color intensity and pattern, fruit sugar content, and resistance to fungal diseases. We anticipate that utilization of this integrated resource will enhance genetic dissection of important traits and accelerate melon breeding.

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

The Pace of Life: Metabolic Energy, Biological Time, and Life History.

New biophysical theory and electronic databases raise the prospect of deriving fundamental rules of life, a conceptual framework for how the structures and functions of molecules, cells and individual organisms give rise to emergent patterns and processes of ecology, evolution and biodiversity. This framework is very general, applying across taxa of animals from 10-10 g protists to 108 g whales, and across environments from deserts and abyssal depths to rain forests and coral reefs. It has several hallmarks: 1) Energy is the ultimate limiting resource for organisms and the currency of biological fitness. 2) Most organisms are nearly equally fit, because in each generation at steady state they transfer an equal quantity of energy (22.4 kJ/g) and biomass (1 g/g) to surviving offspring. This is the equal fitness paradigm (EFP) of Brown et al. (2018). 3) The enormous diversity of life histories is due largely to variation in metabolic rates (e.g., energy uptake and expenditure via assimilation, respiration and production) and biological times (e.g., generation time). As in standard allometric and metabolic theory, most physiological and life history traits scale approximately as quarter-power functions of body mass, m (rates as ∼m-1/4 and times as ∼m1/4), and as exponential functions of temperature. 4) Time is the fourth dimension of life. Generation time is the pace of life. 5) There is, however, considerable variation not accounted for by the above scalings and existing theories. Much of this "unexplained" variation is due to natural selection on life history traits to adapt the biological times of generations to the clock times of geochronological environmental cycles. 7) Most work on biological scaling and metabolic ecology has focused on respiration rate. The emerging synthesis applies conceptual foundations of energetics and the EFP to shift the focus to production rate and generation time.

QTL mapping and genomic analyses of earliness and fruit ripening traits in a melon Recombinant Inbred Lines population supported by de novo assembly of their parental genomes.

Earliness and ripening behavior are important attributes of fruits on and off the vine, and affect quality and preference of both growers and consumers. Fruit ripening is a complex physiological process that involves metabolic shifts affecting fruit color, firmness, and aroma production. Melon is a promising model crop for the study of fruit ripening, as the full spectrum of climacteric behavior is represented across the natural variation. Using Recombinant Inbred Lines (RILs) population derived from the parental lines "Dulce" (reticulatus, climacteric) and "Tam Dew" (inodorus, non-climacteric) that vary in earliness and ripening traits, we mapped QTLs for ethylene emission, fruit firmness and days to flowering and maturity. To further annotate the main QTL intervals and identify candidate genes, we used Oxford Nanopore long-read sequencing in combination with Illumina short-read resequencing, to assemble the parental genomes de-novo. In addition to 2.5 million genome-wide SNPs and short InDels detected between the parents, we also highlight here the structural variation between these lines and the reference melon genome. Through systematic multi-layered prioritization process, we identified 18 potential polymorphisms in candidate genes within multi-trait QTLs. The associations of selected SNPs with earliness and ripening traits were further validated across a panel of 177 diverse melon accessions and across a diallel population of 190 F1 hybrids derived from a core subset of 20 diverse parents. The combination of advanced genomic tools with diverse germplasm and targeted mapping populations is demonstrated as a way to leverage forward genetics strategies to dissect complex horticulturally important traits.

How deregulation, drought and increasing fire impact Amazonian biodiversity.

Biodiversity contributes to the ecological and climatic stability of the Amazon Basin1,2, but is increasingly threatened by deforestation and fire3,4. Here we quantify these impacts over the past two decades using remote-sensing estimates of fire and deforestation and comprehensive range estimates of 11,514 plant species and 3,079 vertebrate species in the Amazon. Deforestation has led to large amounts of habitat loss, and fires further exacerbate this already substantial impact on Amazonian biodiversity. Since 2001, 103,079-189,755 km2 of Amazon rainforest has been impacted by fires, potentially impacting the ranges of 77.3-85.2% of species that are listed as threatened in this region5. The impacts of fire on the ranges of species in Amazonia could be as high as 64%, and greater impacts are typically associated with species that have restricted ranges. We find close associations between forest policy, fire-impacted forest area and their potential impacts on biodiversity. In Brazil, forest policies that were initiated in the mid-2000s corresponded to reduced rates of burning. However, relaxed enforcement of these policies in 2019 has seemingly begun to reverse this trend: approximately 4,253-10,343 km2 of forest has been impacted by fire, leading to some of the most severe potential impacts on biodiversity since 2009. These results highlight the critical role of policy enforcement in the preservation of biodiversity in the Amazon.

Areas of global importance for conserving terrestrial biodiversity, carbon and water.

To meet the ambitious objectives of biodiversity and climate conventions, the international community requires clarity on how these objectives can be operationalized spatially and how multiple targets can be pursued concurrently. To support goal setting and the implementation of international strategies and action plans, spatial guidance is needed to identify which land areas have the potential to generate the greatest synergies between conserving biodiversity and nature's contributions to people. Here we present results from a joint optimization that minimizes the number of threatened species, maximizes carbon retention and water quality regulation, and ranks terrestrial conservation priorities globally. We found that selecting the top-ranked 30% and 50% of terrestrial land area would conserve respectively 60.7% and 85.3% of the estimated total carbon stock and 66% and 89.8% of all clean water, in addition to meeting conservation targets for 57.9% and 79% of all species considered. Our data and prioritization further suggest that adequately conserving all species considered (vertebrates and plants) would require giving conservation attention to ~70% of the terrestrial land surface. If priority was given to biodiversity only, managing 30% of optimally located land area for conservation may be sufficient to meet conservation targets for 81.3% of the terrestrial plant and vertebrate species considered. Our results provide a global assessment of where land could be optimally managed for conservation. We discuss how such a spatial prioritization framework can support the implementation of the biodiversity and climate conventions.

Underground heterosis for yield improvement in melon.

Heterosis, the superiority of hybrids over their parents, is a major genetic force associated with plant fitness and crop yield enhancement. We investigated root-mediated yield heterosis in melons (Cucumis melo) by characterizing a common variety grafted onto 190 hybrid rootstocks, resulting from crossing 20 diverse inbreds in a diallel-mating scheme. Hybrid rootstocks improved yield by more than 40% compared with their parents, and the best hybrid yield outperformed the reference commercial variety by 65% under both optimal and minimal irrigation treatments. To characterize the genetics of underground heterosis we conducted whole genome re-sequencing of the 20 founder lines, and showed that parental genetic distance was no predictor for the level of heterosis. Through inference of the 190 hybrid genotypes from their parental genomes, followed by genome-wide association analysis, we mapped multiple quantitative trait loci for root-mediated yield. Yield enhancement of the four best-performing hybrid rootstocks was validated in multiple experiments with four different scion varieties. Our grafting approach is complementary to the common roots genetic approach that focuses mainly on variation in root system architecture, and is a step towards discovery of candidate genes involved in root function and yield enhancement.

Comparative transcriptome analyses shed light on carotenoid production and plastid development in melon fruit.

Carotenoids, such as ß-carotene, accumulate in chromoplasts of various fleshy fruits, awarding them with colors, aromas, and nutrients. The Orange (CmOr) gene controls ß-carotene accumulation in melon fruit by posttranslationally enhancing carotenogenesis and repressing ß-carotene turnover in chromoplasts. Carotenoid isomerase (CRTISO) isomerizes yellow prolycopene into red lycopene, a prerequisite for further metabolism into ß-carotene. We comparatively analyzed the developing fruit transcriptomes of orange-colored melon and its two isogenic EMS-induced mutants, low-ß (Cmor) and yofi (Cmcrtiso). The Cmor mutation in low-ß caused a major transcriptomic change in the mature fruit. In contrast, the Cmcrtiso mutation in yofi significantly changed the transcriptome only in early fruit developmental stages. These findings indicate that melon fruit transcriptome is primarily altered by changes in carotenoid metabolic flux and plastid conversion, but minimally by carotenoid composition in the ripe fruit. Clustering of the differentially expressed genes into functional groups revealed an association between fruit carotenoid metabolic flux with the maintenance of the photosynthetic apparatus in fruit chloroplasts. Moreover, large numbers of thylakoid localized photosynthetic genes were differentially expressed in low-ß. CmOR family proteins were found to physically interact with light-harvesting chlorophyll a-b binding proteins, suggesting a new role of CmOR for chloroplast maintenance in melon fruit. This study brings more insights into the cellular and metabolic processes associated with fruit carotenoid accumulation in melon fruit and reveals a new maintenance mechanism of the photosynthetic apparatus for plastid development.

Universal rules of life: metabolic rates, biological times and the equal fitness paradigm.

Here we review and extend the equal fitness paradigm (EFP) as an important step in developing and testing a synthetic theory of ecology and evolution based on energy and metabolism. The EFP states that all organisms are equally fit at steady state, because they allocate the same quantity of energy, ~ 22.4 kJ/g/generation to the production of offspring. On the one hand, the EFP may seem tautological, because equal fitness is necessary for the origin and persistence of biodiversity. On the other hand, the EFP reflects universal laws of life: how biological metabolism - the uptake, transformation and allocation of energy - links ecological and evolutionary patterns and processes across levels of organisation from: (1) structure and function of individual organisms, (2) life history and dynamics of populations, and (3) interactions and coevolution of species in ecosystems. The physics and biology of metabolism have facilitated the evolution of millions of species with idiosyncratic anatomy, physiology, behaviour and ecology but also with many shared traits and tradeoffs that reflect the single origin and universal rules of life.

Underappreciated plant vulnerabilities to heat waves.

With climate change, heat waves are becoming increasingly frequent, intense and broader in spatial extent. However, while the lethal effects of heat waves on humans are well documented, the impacts on flora are less well understood, perhaps except for crops. We summarize recent findings related to heat wave impacts including: sublethal and lethal effects at leaf and plant scales, secondary ecosystem effects, and more complex impacts such as increased heat wave frequency across all seasons, and interactions with other disturbances. We propose generalizable practical trials to quantify the critical bounding conditions of vulnerability to heat waves. Collectively, plant vulnerabilities to heat waves appear to be underappreciated and understudied, particularly with respect to understanding heat wave driven plant die-off and ecosystem tipping points.

Urban Biodiversity and the Importance of Scale.

Many ecological and evolutionary processes are affected by urbanization, but cities vary by orders of magnitude in their human population size and areal extent. To quantify and manage urban biodiversity, one must understand both how biodiversity scales with city size, and how ecological, evolutionary, and socioeconomic drivers of biodiversity scale with city size. We show how environmental abiotic and biotic drivers, as well as human cultural and socioeconomic drivers, may act through ecological and evolutionary processes differently, at different scales, to influence patterns in urban biodiversity. Because relationships likely take linear and nonlinear forms, the need to describe the specific scaling relationships is highlighted, including deviations and potential inflection points, where different management strategies may successfully conserve urban biodiversity.

Social determinants of health and survival in humans and other animals.

The social environment, both in early life and adulthood, is one of the strongest predictors of morbidity and mortality risk in humans. Evidence from long-term studies of other social mammals indicates that this relationship is similar across many species. In addition, experimental studies show that social interactions can causally alter animal physiology, disease risk, and life span itself. These findings highlight the importance of the social environment to health and mortality as well as Darwinian fitness-outcomes of interest to social scientists and biologists alike. They thus emphasize the utility of cross-species analysis for understanding the predictors of, and mechanisms underlying, social gradients in health.

High-density NGS-based map construction and genetic dissection of fruit shape and rind netting in Cucumis melo.

Melon is an important crop that exhibits broad variation for fruit morphology traits that are the substrate for genetic mapping efforts. In the post-genomic era, the link between genetic maps and physical genome assemblies is key for leveraging QTL mapping results for gene cloning and breeding purposes. Here, using a population of 164 melon recombinant inbred lines (RILs) that were subjected to genotyping-by-sequencing, we constructed and compared high-density sequence- and linkage-based recombination maps that were aligned to the reference melon genome. These analyses reveal the genome-wide variation in recombination frequency and highlight regions of disrupted collinearity between our population and the reference genome. The population was phenotyped over 3 years for fruit size and shape as well as rind netting. Four QTLs were detected for fruit size, and they act in an additive manner, while significant epistatic interaction was found between two neutral loci for this trait. Fruit shape displayed transgressive segregation that was explained by the action of four QTLs, contributed by alleles from both parents. The complexity of rind netting was demonstrated on a collection of 177 diverse accessions. Further dissection of netting in our RILs population, which is derived from a cross of smooth and densely netted parents, confirmed the intricacy of this trait and the involvement of major locus and several other interacting QTLs. A major netting QTL on chromosome 2 co-localized with results from two additional populations, paving the way for future study toward identification of a causative gene for this trait.

The commonness of rarity: Global and future distribution of rarity across land plants.

A key feature of life's diversity is that some species are common but many more are rare. Nonetheless, at global scales, we do not know what fraction of biodiversity consists of rare species. Here, we present the largest compilation of global plant diversity to quantify the fraction of Earth's plant biodiversity that are rare. A large fraction, ~36.5% of Earth's ~435,000 plant species, are exceedingly rare. Sampling biases and prominent models, such as neutral theory and the k-niche model, cannot account for the observed prevalence of rarity. Our results indicate that (i) climatically more stable regions have harbored rare species and hence a large fraction of Earth's plant species via reduced extinction risk but that (ii) climate change and human land use are now disproportionately impacting rare species. Estimates of global species abundance distributions have important implications for risk assessments and conservation planning in this era of rapid global change.

Toward a metabolic theory of life history.

The life histories of animals reflect the allocation of metabolic energy to traits that determine fitness and the pace of living. Here, we extend metabolic theories to address how demography and mass-energy balance constrain allocation of biomass to survival, growth, and reproduction over a life cycle of one generation. We first present data for diverse kinds of animals showing empirical patterns of variation in life-history traits. These patterns are predicted by theory that highlights the effects of 2 fundamental biophysical constraints: demography on number and mortality of offspring; and mass-energy balance on allocation of energy to growth and reproduction. These constraints impose 2 fundamental trade-offs on allocation of assimilated biomass energy to production: between number and size of offspring, and between parental investment and offspring growth. Evolution has generated enormous diversity of body sizes, morphologies, physiologies, ecologies, and life histories across the millions of animal, plant, and microbe species, yet simple rules specified by general equations highlight the underlying unity of life.

The Role of Carotenogenic Metabolic Flux in Carotenoid Accumulation and Chromoplast Differentiation: Lessons From the Melon Fruit.

Carotenoids have various roles in plant physiology. Plant carotenoids are synthesized in plastids and are highly abundant in the chromoplasts of ripening fleshy fruits. Considerable research efforts have been devoted to elucidating mechanisms that regulate carotenoid biosynthesis, yet, little is known about the mechanism that triggers storage capacity, mainly through chromoplast differentiation. The Orange gene (OR) product stabilizes phytoene synthase protein (PSY) and triggers chromoplast differentiation. OR underlies carotenoid accumulation in orange cauliflower and melon. The OR's 'golden SNP', found in melon, alters the highly evolutionary conserved Arginine108 to Histidine and controls ß-carotene accumulation in melon fruit, in a mechanism yet to be elucidated. We have recently shown that similar carotenogenic metabolic flux is active in non-orange and orange melon fruit. This flux probably leads to carotenoid turnover but known carotenoid turnover products are not detected in non-orange fruit. Arrest of this metabolic flux, using chemical inhibitors or mutations, induces carotenoid accumulation and biogenesis of chromoplasts, regardless of the allelic state of OR. We suggest that the 'golden SNP' induces ß-carotene accumulation probably by negatively affecting the capacity to synthesize downstream compounds. The accumulation of carotenoids induces chromoplast biogenesis through a metabolite-induced mechanism. Carotenogenic turnover flux can occur in non-photosynthetic tissues, which do not accumulate carotenoids. Arrest of this flux by the 'golden SNP' or other flux-arrest mutations is a potential tool for the biofortification of agricultural products with carotenoids.

The multi-allelic APRR2 gene is associated with fruit pigment accumulation in melon and watermelon.

Color and pigment contents are important aspects of fruit quality and consumer acceptance of cucurbit crops. Here, we describe the independent mapping and cloning of a common causative APRR2 gene regulating pigment accumulation in melon and watermelon. We initially show that the APRR2 transcription factor is causative for the qualitative difference between dark and light green rind in both crops. Further analyses establish the link between sequence or expression level variations in the CmAPRR2 gene and pigment content in the rind and flesh of mature melon fruits. A genome-wide association study (GWAS) of young fruit rind color in a panel composed of 177 diverse melon accessions did not result in any significant association, leading to an earlier assumption that multiple genes are involved in shaping the overall phenotypic variation in this trait. Through resequencing of 25 representative accessions and allelism tests between light rind accessions, we show that multiple independent single nucleotide polymorphisms in the CmAPRR2 gene are causative of the light rind phenotype. The multi-haplotypic nature of this gene explains the lack of detection power obtained through genotyping by sequencing-based GWAS and confirms the pivotal role of this gene in shaping fruit color variation in melon. This study demonstrates the power of combining bi- and multi-allelic designs with deep sequencing, to resolve lack of power due to high haplotypic diversity and low allele frequencies. Due to its central role and broad effect on pigment accumulation in fruits, the APRR2 gene is an attractive target for carotenoid bio-fortification of cucurbit crops.