Assembly and analysis of the genome of Notholithocarpus densiflorus.

Tanoak (Notholithocarpus densiflorus) is an evergreen tree in the Fagaceae family found in California and southern Oregon. Historically, tanoak acorns were an important food source for Native American tribes and the bark was used extensively in the leather tanning process. Long considered a disjunct relictual element of the Asian stone oaks (Lithocarpus spp.), phylogenetic analysis has determined that the tanoak is an example of convergent evolution. Tanoaks are deeply divergent from oaks (Quercus) of the Pacific Northwest and comprise a new genus with a single species. These trees are highly susceptible to 'sudden oak death' (SOD), a plant pathogen (Phytophthora ramorum) that has caused widespread mortality of tanoaks. Here, we set out to assemble the genome and perform comparative studies among a number of individuals that demonstrated varying levels of susceptibility to SOD. First, we sequenced and de novo assembled a draft reference genome of N. densiflorus using co-barcoded library processing methods and an MGI DNBSEQ-G400 sequencer. To increase the contiguity of the final assembly, we also sequenced Oxford Nanopore (ONT) long reads to 30X coverage. To our knowledge, the draft genome reported here is one of the more contiguous and complete genomes of a tree species published to date, with a contig N50 of ∼1.2 Mb, a scaffold N50 of ∼2.1 Mb, and a complete gene score of 95.5% through BUSCO analysis. In addition, we sequenced 11 genetically distinct individuals and mapped these onto the draft reference genome enabling the discovery of almost 25 million single nucleotide polymorphisms and ∼4.4 million small insertions and deletions. Finally, using co-barcoded data we were able to generate complete haplotype coverage of all 11 genomes.

The magmatic origin of the Columbia River Gorge, USA.

Along subduction zones, high-relief topography is associated with sustained volcanism parallel to the plate margin. However, the relationship between magmatism and mountain building in arcs is poorly understood. Here, we study patterns of surface deformation and correlated fluvial knickpoints in the Columbia River Gorge to link long-term magmatism to the uplift and ensuing topographic development of the Cascade Range. An upwarped paleochannel exposed in the walls of the Gorge constrains unsteady deep magma flux, the ratio of intrusive to extrusive magmatic contributions to topography, and the impact of magmatism on Columbia River incision since 3.5 million years ago. Geophysical data indicate that deep magma influx beneath the arc axis is ongoing and not aligned with the current locations of volcanic edifices, representing a broad regional influence on arc construction.

Virtually the Same? Evaluating the Effectiveness of Remote Undergraduate Research Experiences.

In-person undergraduate research experiences (UREs) promote students' integration into careers in life science research. In 2020, the COVID-19 pandemic prompted institutions hosting summer URE programs to offer them remotely, raising questions about whether undergraduates who participate in remote research can experience scientific integration and whether they might perceive doing research less favorably (i.e., not beneficial or too costly). To address these questions, we examined indicators of scientific integration and perceptions of the benefits and costs of doing research among students who participated in remote life science URE programs in Summer 2020. We found that students experienced gains in scientific self-efficacy pre- to post-URE, similar to results reported for in-person UREs. We also found that students experienced gains in scientific identity, graduate and career intentions, and perceptions of the benefits of doing research only if they started their remote UREs at lower levels on these variables. Collectively, students did not change in their perceptions of the costs of doing research despite the challenges of working remotely. Yet students who started with low cost perceptions increased in these perceptions. These findings indicate that remote UREs can support students' self-efficacy development, but may otherwise be limited in their potential to promote scientific integration.

Ancient trees: irreplaceable conservation resource for ecosystem restoration.

Ancient trees contribute multifaceted ecosystem benefits to old-growth forests, rewilding, and human cultural landscapes. As such, we call for international efforts to preserve these hubs of diversity and resilience. A global coalition utilizing advanced technologies and community scientists to discover, protect, and propagate ancient trees is needed before they disappear.

Old and ancient trees are life history lottery winners and vital evolutionary resources for long-term adaptive capacity.

Trees can live for many centuries with sustained fecundity and death is largely stochastic. We use a neutral stochastic model to examine tree demographic patterns that emerge over time, across a range of population sizes and empirically observed mortality rates. A small proportion of trees (~1% at 1.5% mortality) are life-history 'lottery winners', achieving ages >10-20× the median age. Maximum age increases with bigger populations and lower mortality rates. One-quarter of trees (~24%) achieve ages that are three to four times greater than the median age. Three age classes (mature, old and ancient) contribute unique evolutionary diversity across complex environmental cycles. Ancient trees are an emergent property of forests that requires many centuries to generate. They radically change variance in generation time and population fitness, bridging centennial environmental cycles. These life-history 'lottery' winners are vital to long-term forest adaptive capacity and provide invaluable data about environmental history and individual longevity. Old and ancient trees cannot be replaced through restoration or regeneration for many centuries. They must be protected to preserve their invaluable diversity.

"How Do We Do This at a Distance?!" A Descriptive Study of Remote Undergraduate Research Programs during COVID-19.

The COVID-19 pandemic shut down undergraduate research programs across the United States. A group of 23 colleges, universities, and research institutes hosted remote undergraduate research programs in the life sciences during Summer 2020. Given the unprecedented offering of remote programs, we carried out a study to describe and evaluate them. Using structured templates, we documented how programs were designed and implemented, including who participated. Through focus groups and surveys, we identified programmatic strengths and shortcomings as well as recommendations for improvements from students' perspectives. Strengths included the quality of mentorship, opportunities for learning and professional development, and a feeling of connection with a larger community. Weaknesses included limited cohort building, challenges with insufficient structure, and issues with technology. Although all programs had one or more activities related to diversity, equity, inclusion, and justice, these topics were largely absent from student reports even though programs coincided with a peak in national consciousness about racial inequities and structural racism. Our results provide evidence for designing remote Research Experiences for Undergraduates (REUs) that are experienced favorably by students. Our results also indicate that remote REUs are sufficiently positive to further investigate their affordances and constraints, including the potential to scale up offerings, with minimal concern about disenfranchising students.

Is speciation an unrelenting march to reproductive isolation?

Speciation is often portrayed as an "incomplete" or "incipient" process if two groups of organisms, technically distinguishable either by morphology or genetics, can exchange genes. The ultimate outcome of diversification, given this perspective, is complete reproductive isolation. But an increasing amount of evidence suggests that speciation is rarely complete and inter-fertility between different taxonomically accepted species is consistently maintained. In this issue of Molecular Ecology, Linan et al. (2021) provide results that bridge evolutionary processes from populations to phylogenies that indicate suites of closely related tree species in the Mascarene Islands actively exchange genes, evolving as a nested set of syngameons with a hierarchical pattern of interfertility. The deep insight into diversification provided by this study is particularly powerful because of the genomic scale of the data and the complete taxonomic sampling of an island clade evolving in situ. The prevalence of syngameon dynamics in a broad range of organisms indicates that we should adopt a fluid and comprehensive approach to defining evolutionary units for conservation and research. We should move beyond focusing on single endangered species in evolutionary and ecological isolation from other species but consider the entire network of potentially interfertile species and the potential for future adaptation and innovation, particularly in a human dominated world.

Discovering and Applying the Urban Rules of Life to Design Sustainable and Healthy Cities.

The city and its urban biome provides an extreme laboratory for studying fundamental biological questions and developing best practices for sustaining biodiverse and well-functioning ecological communities within anthropogenic built environments. We propose by studying urban organisms, urban biotic communities, the urban biome, and the interactions between the urban biome and peri-urban built and natural environments, we can (1) discover new "rules of life" for the structure, function, interaction, and evolution of organisms; (2) use these discoveries to understand how novel emerging biotic communities affect and are affected by anthropogenic environmental changes in climate and other environmental factors; and (3) apply what we have learned to engage residents of the urban biome, and design cities that are more biologically diverse, are provided with more and better ecosystem services, and are more equitable and healthier places to live. The built environment of the urban biome is a place that reflects history, economics, technology, governance, culture, and values of the human residents; research on and applications of the rules of life in the urban biome can be used by all residents in making choices about the design of the cities where they live. Because inhabitants are directly invested in the environmental quality of their neighborhoods, research conducted in and about the urban environment provides a great opportunity to engage wide and diverse communities of people. Given the opportunity to engage a broad constituency-from basic researchers to teachers, civil engineers, landscape planners, and concerned citizens-studying the translation of the rules of life onto the urban environment will result in an integrative and cross-cutting set of questions and hypotheses, and will foster a dialog among citizens about the focus of urban biome research and its application toward making more equitable, healthy, livable, sustainable, and biodiverse cities.

Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism.

Ficus (figs) and their agaonid wasp pollinators present an ecologically important mutualism that also provides a rich comparative system for studying functional co-diversification throughout its coevolutionary history (~75 million years). We obtained entire nuclear, mitochondrial, and chloroplast genomes for 15 species representing all major clades of Ficus. Multiple analyses of these genomic data suggest that hybridization events have occurred throughout Ficus evolutionary history. Furthermore, cophylogenetic reconciliation analyses detect significant incongruence among all nuclear, chloroplast, and mitochondrial-based phylogenies, none of which correspond with any published phylogenies of the associated pollinator wasps. These findings are most consistent with frequent host-switching by the pollinators, leading to fig hybridization, even between distantly related clades. Here, we suggest that these pollinator host-switches and fig hybridization events are a dominant feature of fig/wasp coevolutionary history, and by generating novel genomic combinations in the figs have likely contributed to the remarkable diversity exhibited by this mutualism.

Application of remote sensing technology to estimate productivity and assess phylogenetic heritability.

PREMISE: Measuring plant productivity is critical to understanding complex community interactions. Many traditional methods for estimating productivity, such as direct measurements of biomass and cover, are resource intensive, and remote sensing techniques are emerging as viable alternatives. METHODS: We explore drone-based remote sensing tools to estimate productivity in a tallgrass prairie restoration experiment and evaluate their ability to predict direct measures of productivity. We apply these various productivity measures to trace the evolution of plant productivity and the traits underlying it. RESULTS: The correlation between remote sensing data and direct measurements of productivity varies depending on vegetation diversity, but the volume of vegetation estimated from drone-based photogrammetry is among the best predictors of biomass and cover regardless of community composition. The commonly used normalized difference vegetation index (NDVI) is a less accurate predictor of biomass and cover than other equally accessible vegetation indices. We found that the traits most strongly correlated with productivity have lower phylogenetic signal, reflecting the fact that high productivity is convergent across the phylogeny of prairie species. This history of trait convergence connects phylogenetic diversity to plant community assembly and succession. DISCUSSION: Our study demonstrates (1) the importance of considering phylogenetic diversity when setting management goals in a threatened North American grassland ecosystem and (2) the utility of remote sensing as a complement to ground measurements of grassland productivity for both applied and fundamental questions.

Fruit development of Lithocarpus (Fagaceae) and the role of heterochrony in their evolution.

Stone oaks, or Lithocarpus species of Fagaceae are ecologically important canopy trees in the tropical and subtropical forests over East Asia, and the fruits of which are important food sources for insects and vertebrates there. The great fruit morphological variation of this genus represents two fruit types, acorn and enclosed receptacle fruit types. However, the evolutionary mechanisms of differentiation into these two fruit types with contrasting morphology remain a puzzle. To reveal the morphogenetic properties of two fruit types, we observed tissue differentiation and development among 20 Lithocarpus species from fruit set to maturity. Unlike in fruits of Quercus, the endocarp differentiation in Lithocarpus fruits occurred later than exocarp and mesocarp. Cupules provided further protection of developing seeds, particularly of acorn-type fruits. Fruits of Lithocarpus and Quercus acorns share similar insect predators. At fruit set, both acorn and enclosed receptacle types were largely identical, with similar tissue morphology and the sequence of differentiation. The distinct difference between two fruit types at maturity came from varied rates and degrees of development between the pericarp and receptacle tissues. We found that heterochrony between two tissues could create substantially divergent ecological strategies for protection and dispersal of their seeds, which is essential for the evolution of two fruit types.

The oak syngameon: more than the sum of its parts.

One of Anthropocene's most daunting challenges for conservation biology is habitat extinction, caused by rapid global change. Tree diversity has persisted through previous episodes of rapid change, even global extinctions. Given the pace of current change, our management of extant diversity needs to facilitate and even enhance the natural ability of trees to adapt and diversify. Numerous processes contribute to this evolutionary flexibility, including introgression, a widespread yet under-studied process. Reproductive networks, in which species remain distinct despite interspecific gene flow, are called syngameons, a concept largely inspired from work focusing on Quercus. Delineating and analyzing such species groups, empirically and theoretically, will provide insights into the nonadditive effects on evolution of numerous partially interfertile species exchanging genetic material episodically under changing environmental conditions. To conserve tree diversity, crossing experiments designed with an empirical and theoretical understanding of the constituent syngameon should be set up to assist diversification and adaptation in the Anthropocene. Our increasingly detailed knowledge of the oak genome and of oak interspecific and intraspecific phenotypic variation will improve our ability to sustain the diversity of this tree through an unpredictable and unprecedented future.

Correction: Associated morphometric and geospatial differentiation among 98 species of stone oaks (Lithocarpus).

[This corrects the article DOI: 10.1371/journal.pone.0199538.].

Associated morphometric and geospatial differentiation among 98 species of stone oaks (Lithocarpus).

Two fruit types can be distinguished among stone oaks (Lithocarpus) species: the 'acorn' (AC) and the 'enclosed receptacle' (ER) types. Our morphometric analysis of 595 nuts from 98 species (one third of all Lithocarpus spp.) found substantial transition in mechanical protection of the seed between two woody fruit tissues (exocarp and receptacle) of two fruit types. AC fruits were smaller in seed and fruit size and the thin brittle exocarp largely enclosed the seed, whereas ER fruits were larger and the seed was mostly enclosed by thick woody receptacle tissue. The differences in these two tissues were considerably greater between compared to within fruit type and species. Geospatial distribution showed that seed size of all examined species increased with elevation and decreased with latitude, the physical defense increased with both elevation and latitude, and ER-fruit species were more common at higher elevation. The two fruit types represent distinct suites of associated traits that respond differently to the various biotic and abiotic factors associated with geographic variation, profoundly impacting the evolution of the two fruit types. The co-occurrence of two fruit types in the same forest could be a consequence of distinct fruit and animal interactions.

Exploring the potential of gametic reconstruction of parental genotypes by F1 hybrids as a bridge for rapid introgression.

Interspecific hybridization and genetic introgression are commonly observed in natural populations of many species, especially trees. Among oaks, gene flow between closely related species has been well documented. And yet, hybridization does not lead to a "melting pot", i.e., the homogenization of phenotypic traits. Here, we explore how the combination of several common reproductive and genomic traits could create an avenue for interspecific gene flow that partially explains this apparent paradox. During meiosis, F1 hybrids will produce approximately (½)n "reconstructed" parental gametes, where n equals the number of chromosomes. Crossing over would introduce a small amount of introgressive material. The resulting parental-type gametophytes would probably possess a similar fertilization advantage as conspecific pollen. The resulting "backcross" would actually be the genetic equivalent of a conspecific out-cross, with a small amount of heterospecific DNA captured through crossing over. Even with detailed genomic analysis, the resulting offspring would not appear to be a backcross. This avenue for rapid introgression between species through the F1 hybrid will be viable for organisms that meet certain conditions: low base chromosome number, conserved genomic structure and size, production of billions of gametes/gametophytes during each reproductive event, and conspecific fertilization advantage.

Patterns of genomic diversification reflect differences in life history and reproductive biology between figs (Ficus) and the stone oaks (Lithocarpus).

One of the remarkable aspects of the tremendous biodiversity found in tropical forests is the wide range of evolutionary strategies that have produced this diversity, indicating many paths to diversification. We compare two diverse groups of trees with profoundly different biologies to discover whether these differences are reflected in their genomes. Ficus (Moraceae), with its complex co-evolutionary relationship with obligate pollinating wasps, produces copious tiny seeds that are widely dispersed. Lithocarpus (Fagaceae), with generalized insect pollination, produces large seeds that are poorly dispersed. We hypothesize that these different reproductive biologies and life history strategies should have a profound impact on the basic properties of genomic divergence within each genus. Using shallow whole genome sequencing for six species of Ficus, seven species of Lithocarpus, and three outgroups, we examined overall genomic diversity, how it is shared among the species within each genus, and the fraction of this shared diversity that agrees with the major phylogenetic pattern. A substantially larger fraction of the genome is shared among species of Lithocarpus, a considerable amount of this shared diversity was incongruent with the general background history of the genomes, and each fig species possessed a substantially larger fraction of unique diversity than Lithocarpus.