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Key Points Polyploidy, or whole-genome duplication (WGD), is usually an evolutionary dead end. Although polyploidy is a frequent and recurrent phenomenon, the number of WGDs that have become established in the long term is low. The occurrence of WGDs in the tree of life is not random and seems to correlate with periods of environmental upheaval. WGDs increase the adaptive potential of cells and organisms exposed to stressful conditions. The biased retention of genes following WGDs offers a unique evolutionary potential to evolve key innovations and to increase biological complexity in the long term. In cancer, WGD is a transient state that promotes aneuploidy, and is responsible for increased genetic variation and subsequent adaptive potential. Polyploidy occurs frequently but is usually detrimental to survival; thus, few polyploids survive in the long term. Here, evidence linking the short-term evolutionary success of polyploids to environmental upheaval is reviewed and possible longer-term evolutionary benefits of polyploidy are discussed. Polyploidy, or the duplication of entire genomes, has been observed in prokaryotic and eukaryotic organisms, and in somatic and germ cells. The consequences of polyploidization are complex and variable, and they differ greatly between systems (clonal or non-clonal) and species, but the process has often been considered to be an evolutionary 'dead end'. Here, we review the accumulating evidence that correlates polyploidization with environmental change or stress, and that has led to an increased recognition of its short-term adaptive potential. In addition, we discuss how, once polyploidy has been established, the unique retention profile of duplicated genes following whole-genome duplication might explain key longer-term evolutionary transitions and a general increase in biological complexity.

The microbiome shapes many host traits, yet the biology of microbiomes challenges traditional evolutionary models. Here, we illustrate how integrating the microbiome into quantitative genetics can help untangle complexities of host-microbiome evolution. We describe two general ways in which the microbiome may affect host evolutionary potential: by shifting the mean host phenotype and by changing the variance in host phenotype in the population. We synthesize the literature across diverse taxa and discuss how these scenarios could shape the host response to selection. We conclude by outlining key avenues of research to improve our understanding of the complex interplay between hosts and microbiomes. The microbiome is becoming recognized as a key determinant of host phenotype. Here, Henry et al. present a framework for building our understanding of how the microbiome also influences host evolution, review empirical examples and research approaches, and highlight emerging questions.

Strategic interactions arise in all domains of life. This form of competition often plays out in dynamically changing environments. The strategies employed in a population may alter the state of the environment, which may in turn feedback to change the incentive structure of strategic interactions. Feedbacks between strategies and the environment are common in social-ecological systems, evolutionary-ecological systems, and even psychological-economic systems. Here we develop a framework of ‘eco-evolutionary game theory’ that enables the study of strategic and environmental dynamics with feedbacks. We consider environments governed either by intrinsic growth, decay, or tipping points. We show how the joint dynamics of strategies and the environment depend on the incentives for individuals to lead or follow behavioral changes, and on the relative speed of environmental versus strategic change. Our analysis unites dynamical phenomena that occur in settings as diverse as human decision-making, plant nutrient acquisition, and resource harvesting. We discuss implications in fields ranging from ecology to economics. Strategic game payoffs often depend on the state of the environment, which in turn can be influenced by game strategies. Here, Tilman et al. develop a general framework for modeling strategic games with environmental feedbacks and analyze case studies from decision-making, ecology, and economics.

A dated phylogeny and spatial distribution data for Chinese angiosperms show that eastern China has tended to act as a refugium for older taxa whereas western China has acted as a centre for their evolutionary diversification. A blossoming history of Chinese flora China is home to a vast range of flowering plants and has been seen as both a refuge for ancient lineages and a cradle for recent ones. Zhi-Duan Chen and colleagues examine the evolutionary history of Chinese flora and conclude that it is indeed both refuge and birthplace, but with a geographical twist. They find that 66% of Chinese flowering plant genera did not originate until the early Miocene (23 million years ago), but also uncover a distinct split between western and eastern China. Whereas lush, lowland eastern China tends to offer refuge for older genera, the rugged heights and harsh deserts of the west tend to be cradles for new evolutionary diversity. High species diversity may result from recent rapid speciation in a ‘cradle’ and/or the gradual accumulation and preservation of species over time in a ‘museum’ 1 , 2 . China harbours nearly 10% of angiosperm species worldwide and has long been considered as both a museum, owing to the presence of many species with hypothesized ancient origins 3 , 4 , and a cradle, as many lineages have originated as recent topographic changes and climatic shifts—such as the formation of the Qinghai–Tibetan Plateau and the development of the monsoon—provided new habitats that promoted remarkable radiation 5 . However, no detailed phylogenetic study has addressed when and how the major components of the Chinese angiosperm flora assembled to form the present-day vegetation. Here we investigate the spatio-temporal divergence patterns of the Chinese flora using a dated phylogeny of 92% of the angiosperm genera for the region, a nearly complete species-level tree comprising 26,978 species and detailed spatial distribution data. We found that 66% of the angiosperm genera in China did not originate until early in the Miocene epoch (23 million years ago (Mya)). The flora of eastern China bears a signature of older divergence (mean divergence times of 22.04–25.39 Mya), phylogenetic overdispersion (spatial co-occurrence of distant relatives) and higher phylogenetic diversity. In western China, the flora shows more recent divergence (mean divergence times of 15.29–18.86 Mya), pronounced phylogenetic clustering (co-occurrence of close relatives) and lower phylogenetic diversity. Analyses of species-level phylogenetic diversity using simulated branch lengths yielded results similar to genus-level patterns. Our analyses indicate that eastern China represents a floristic museum, and western China an evolutionary cradle, for herbaceous genera; eastern China has served as both a museum and a cradle for woody genera. These results identify areas of high species richness and phylogenetic diversity, and provide a foundation on which to build conservation efforts in China.

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary ‘attractors’ that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change. Historical climate adaptation can give insight into the potential for adaptation to contemporary changing climates. Here Bennett et al. investigate thermal tolerance evolution across much of the tree of life and find different effects of ancestral climate on the subsequent evolution of ectotherms vs. endotherms.

Climate’s effect on global biodiversity is typically viewed through the lens of temperature, humidity and resulting ecosystem productivity 1 – 6 . However, it is not known whether biodiversity depends solely on these climate conditions, or whether the size and fragmentation of these climates are also crucial. Here we shift the common perspective in global biodiversity studies, transitioning from geographic space to a climate-defined multidimensional space. Our findings suggest that larger and more isolated climate conditions tend to harbour higher diversity and species turnover among terrestrial tetrapods, encompassing more than 30,000 species. By considering both the characteristics of climate itself and its geographic attributes, we can explain almost 90% of the variation in global species richness. Half of the explanatory power (45%) may be attributed either to climate itself or to the geography of climate, suggesting a nuanced interplay between them. Our work evolves the conventional idea that larger climate regions, such as the tropics, host more species primarily because of their size 7 , 8 . Instead, we underscore the integral roles of both the geographic extent and degree of isolation of climates. This refined understanding presents a more intricate picture of biodiversity distribution, which can guide our approach to biodiversity conservation in an ever-changing world. Nearly 90% of global variation in species richness of birds, mammals, amphibians and reptiles is shown to be explained by the joint effects of climate and the geographic structure (area and isolation) of climate.

Late Pliocene and Early Pleistocene epochs 3.6 to 0.8 million years ago 1 had climates resembling those forecasted under future warming 2 . Palaeoclimatic records show strong polar amplification with mean annual temperatures of 11–19 °C above contemporary values 3 , 4 . The biological communities inhabiting the Arctic during this time remain poorly known because fossils are rare 5 . Here we report an ancient environmental DNA 6 (eDNA) record describing the rich plant and animal assemblages of the Kap København Formation in North Greenland, dated to around two million years ago. The record shows an open boreal forest ecosystem with mixed vegetation of poplar, birch and thuja trees, as well as a variety of Arctic and boreal shrubs and herbs, many of which had not previously been detected at the site from macrofossil and pollen records. The DNA record confirms the presence of hare and mitochondrial DNA from animals including mastodons, reindeer, rodents and geese, all ancestral to their present-day and late Pleistocene relatives. The presence of marine species including horseshoe crab and green algae support a warmer climate than today. The reconstructed ecosystem has no modern analogue. The survival of such ancient eDNA probably relates to its binding to mineral surfaces. Our findings open new areas of genetic research, demonstrating that it is possible to track the ecology and evolution of biological communities from two million years ago using ancient eDNA. Analysis of two-million-year-old ancient environmental DNA from the Kap København Formation in North Greenland shows there was an open boreal forest with diverse plant and animal species, of which several taxa have not previously been detected at the site, representing an ecosystem that has no present-day analogue.

In the absence of antibiotic-mediated selection, sensitive bacteria are expected to displace their resistant counterparts if resistance genes are costly. However, many resistance genes persist for long periods in the absence of antibiotics. Horizontal gene transfer (primarily conjugation) could explain this persistence, but it has been suggested that very high conjugation rates would be required. Here, we show that common conjugal plasmids, even when costly, are indeed transferred at sufficiently high rates to be maintained in the absence of antibiotics in Escherichia coli . The notion is applicable to nine plasmids from six major incompatibility groups and mixed populations carrying multiple plasmids. These results suggest that reducing antibiotic use alone is likely insufficient for reversing resistance. Therefore, combining conjugation inhibition and promoting plasmid loss would be an effective strategy to limit conjugation-assisted persistence of antibiotic resistance. It is unclear whether the transfer of plasmids carrying antibiotic resistance genes can explain their persistence when antibiotics are not present. Here, Lopatkin et al. show that conjugal plasmids, even when costly, are indeed transferred at sufficiently high rates to be maintained in the absence of antibiotics.

Analyses of a global dataset of plant root traits identify an ancestral conservative strategy based on thick roots and mycorrhizal symbiosis, and an evolutionarily more-recent opportunistic strategy of thin roots that efficiently use photosynthetic carbon for soil exploration. Unearthing evolution in roots The 'leaf economics spectrum' describes the trade-off that plants make between the energetic and material cost of building a leaf and how long it lasts, but do similar principles govern investment in their roots? The answer seems to be 'yes'. Here, the authors assemble a large database of root traits of 369 species from seven global biomes. The data show that thicker roots tend to be found in more primitive plants such as those in the tropics and those that are sustained through a symbiotic relationship with fungi. Thinner roots are correlated with more recent evolutionary developments and the colonization of temperate and boreal habitats where the supply of nutrients and resources is more seasonal. Plant roots have greatly diversified in form and function since the emergence of the first land plants 1 , 2 , but the global organization of functional traits in roots remains poorly understood 3 , 4 . Here we analyse a global dataset of 10 functionally important root traits in metabolically active first-order roots, collected from 369 species distributed across the natural plant communities of 7 biomes. Our results identify a high degree of organization of root traits across species and biomes, and reveal a pattern that differs from expectations based on previous studies 5 , 6 of leaf traits. Root diameter exerts the strongest influence on root trait variation across plant species, growth forms and biomes. Our analysis suggests that plants have evolved thinner roots since they first emerged in land ecosystems, which has enabled them to markedly improve their efficiency of soil exploration per unit of carbon invested and to reduce their dependence on symbiotic mycorrhizal fungi. We also found that diversity in root morphological traits is greatest in the tropics, where plant diversity is highest and many ancestral phylogenetic groups are preserved. Diversity in root morphology declines sharply across the sequence of tropical, temperate and desert biomes, presumably owing to changes in resource supply caused by seasonally inhospitable abiotic conditions. Our results suggest that root traits have evolved along a spectrum bounded by two contrasting strategies of root life: an ancestral ‘conservative’ strategy in which plants with thick roots depend on symbiosis with mycorrhizal fungi for soil resources and a more-derived ‘opportunistic’ strategy in which thin roots enable plants to more efficiently leverage photosynthetic carbon for soil exploration. These findings imply that innovations of belowground traits have had an important role in preparing plants to colonize new habitats, and in generating biodiversity within and across biomes.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species. It is unclear whether species’ responses to climate change tend to be adaptive or sufficient to keep up with climate change. Here, Radchuk et al. perform a meta-analysis showing that in birds phenology has advanced adaptively in some species, though not all the way to the new optima.