Integrating cultural evolution and behavioral genetics.

The 29 commentaries amplified our key arguments; offered extensions, implications, and applications of the framework; and pushed back and clarified. To help forge the path forward for cultural evolutionary behavioral genetics, we (1) focus on conceptual disagreements and misconceptions about the concepts of heritability and culture; (2) further discuss points raised about the intertwined relationship between culture and genes; and (3) address extensions to the proposed framework, particularly as it relates to cultural clusters, development, and power. These commentaries, and the deep engagement they represent, reinforce the importance of integrating cultural evolution and behavioral genetics.

Cultural evolution of genetic heritability.

Behavioral genetics and cultural evolution have both revolutionized our understanding of human behavior - largely independent of each other. Here, we reconcile these two fields under a dual inheritance framework, offering a more nuanced understanding of the interaction between genes and culture. Going beyond typical analyses of gene-environment interactions, we describe the cultural dynamics that shape these interactions by shaping the environment and population structure. A cultural evolutionary approach can explain, for example, how factors such as rates of innovation and diffusion, density of cultural subgroups, and tolerance for behavioral diversity impact heritability estimates, thus yielding predictions for different social contexts. Moreover, when cumulative culture functionally overlaps with genes, genetic effects become masked, unmasked, or even reversed, and the causal effects of an identified gene become confounded with features of the cultural environment. The manner of confounding is specific to a particular society at a particular time, but a WEIRD (western, educated, industrialized, rich, and democratic) sampling problem obscures this boundedness. Cultural evolutionary dynamics are typically missing from models of gene-to-phenotype causality, hindering generalizability of genetic effects across societies and across time. We lay out a reconciled framework and use it to predict the ways in which heritability should differ between societies, between socioeconomic levels, and other groupings within some societies but not others, and over the life course. An integrated cultural evolutionary behavioral genetic approach cuts through the nature-nurture debate and helps resolve controversies in topics such as IQ.

Differential regulation of auxin and cytokinin during the secondary vascular tissue regeneration in Populus trees.

Tissue regeneration upon wounding in plants highlights the developmental plasticity of plants. Previous studies have described the morphological and molecular changes of secondary vascular tissue (SVT) regeneration after large-scale bark girdling in trees. However, how phytohormones regulate SVT regeneration is still unknown. Here, we established a novel in vitro SVT regeneration system in the hybrid aspen (Populus tremula × Populus tremuloides) clone T89 to bypass the limitation of using field-grown trees. The effects of phytohormones on SVT regeneration were investigated by applying exogenous hormones and utilizing various transgenic trees. Vascular tissue-specific markers and hormonal response factors were also examined during SVT regeneration. Using this in vitro regeneration system, we demonstrated that auxin and cytokinin differentially regulate phloem and cambium regeneration. Whereas auxin is sufficient to induce regeneration of phloem prior to continuous cambium restoration, cytokinin only promotes the formation of new phloem, not cambium. The positive role of cytokinin on phloem regeneration was further confirmed in cytokinin overexpression trees. Analysis of a DR5 reporter transgenic line further suggested that cytokinin blocks the re-establishment of auxin gradients, which is required for the cambium formation. Investigation on the auxin and cytokinin signalling genes indicated these two hormones interact to regulate SVT regeneration. Taken together, the in vitro SVT regeneration system allows us to make use of various molecular and genetic tools to investigate SVT regeneration. Our results confirmed that complementary auxin and cytokinin domains are required for phloem and cambium reconstruction.

Polar auxin transport is implicated in vessel differentiation and spatial patterning during secondary growth in Populus.

PREMISE OF THE STUDY: Dimensions and spatial distribution of vessels are critically important features of woody stems, allowing for adaptation to different environments through their effects on hydraulic efficiency and vulnerability to embolism. Although our understanding of vessel development is poor, basipetal transport of auxin through the cambial zone may play an important role. METHODS: Stems of Populus tremula ×alba were treated with the auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) in a longitudinal strip along the length of the lower stem. Vessel lumen diameter, circularity, and length; xylem growth; tension wood area; and hydraulic conductivity before and after a high pressure flush were determined on both NPA-treated and control plants. KEY RESULTS: NPA-treated stems formed aberrant vessels that were short, small in diameter, highly clustered, and angular in cross section, whereas xylem formed on the untreated side of the stem contained typical vessels that were similar to those of controls. NPA-treated stems had reduced specific conductivity relative to controls, but this difference was eliminated by the high-pressure flush. The control treatment (lanolin + dimethyl sulfoxide) reduced xylem growth and increased tension wood formation, but never produced the aberrant vessel patterning seen in NPA-treated stems. CONCLUSIONS: These results are consistent with a model of vessel development in which basipetal polar auxin transport through the xylem-side cambial derivatives is required for proper expansion and patterning of vessels and demonstrate that reduced auxin transport can produce stems with altered stem hydraulic properties.

A lost opportunity for science: journals promote data sharing in metabolomics but do not enforce it.

INTRODUCTION: Data sharing is being increasingly required by journals and has been heralded as a solution to the 'replication crisis'. OBJECTIVES: (i) Review data sharing policies of journals publishing the most metabolomics papers associated with open data and (ii) compare these journals' policies to those that publish the most metabolomics papers. METHODS: A PubMed search was used to identify metabolomics papers. Metabolomics data repositories were manually searched for linked publications. RESULTS: Journals that support data sharing are not necessarily those with the most papers associated to open metabolomics data. CONCLUSION: Further efforts are required to improve data sharing in metabolomics.

The future of metabolomics in ELIXIR.

Metabolomics, the youngest of the major omics technologies, is supported by an active community of researchers and infrastructure developers across Europe. To coordinate and focus efforts around infrastructure building for metabolomics within Europe, a workshop on the "Future of metabolomics in ELIXIR" was organised at Frankfurt Airport in Germany. This one-day strategic workshop involved representatives of ELIXIR Nodes, members of the PhenoMeNal consortium developing an e-infrastructure that supports workflow-based metabolomics analysis pipelines, and experts from the international metabolomics community. The workshop established metabolite identification as the critical area, where a maximal impact of computational metabolomics and data management on other fields could be achieved. In particular, the existing four ELIXIR Use Cases, where the metabolomics community - both industry and academia - would benefit most, and which could be exhaustively mapped onto the current five ELIXIR Platforms were discussed. This opinion article is a call for support for a new ELIXIR metabolomics Use Case, which aligns with and complements the existing and planned ELIXIR Platforms and Use Cases.

Compliance with minimum information guidelines in public metabolomics repositories.

The Metabolomics Standards Initiative (MSI) guidelines were first published in 2007. These guidelines provided reporting standards for all stages of metabolomics analysis: experimental design, biological context, chemical analysis and data processing. Since 2012, a series of public metabolomics databases and repositories, which accept the deposition of metabolomic datasets, have arisen. In this study, the compliance of 399 public data sets, from four major metabolomics data repositories, to the biological context MSI reporting standards was evaluated. None of the reporting standards were complied with in every publicly available study, although adherence rates varied greatly, from 0 to 97%. The plant minimum reporting standards were the most complied with and the microbial and in vitro were the least. Our results indicate the need for reassessment and revision of the existing MSI reporting standards.

Navigating freely-available software tools for metabolomics analysis.

INTRODUCTION: The field of metabolomics has expanded greatly over the past two decades, both as an experimental science with applications in many areas, as well as in regards to data standards and bioinformatics software tools. The diversity of experimental designs and instrumental technologies used for metabolomics has led to the need for distinct data analysis methods and the development of many software tools. OBJECTIVES: To compile a comprehensive list of the most widely used freely available software and tools that are used primarily in metabolomics. METHODS: The most widely used tools were selected for inclusion in the review by either ≥ 50 citations on Web of Science (as of 08/09/16) or the use of the tool being reported in the recent Metabolomics Society survey. Tools were then categorised by the type of instrumental data (i.e. LC-MS, GC-MS or NMR) and the functionality (i.e. pre- and post-processing, statistical analysis, workflow and other functions) they are designed for. RESULTS: A comprehensive list of the most used tools was compiled. Each tool is discussed within the context of its application domain and in relation to comparable tools of the same domain. An extended list including additional tools is available at https://github.com/RASpicer/MetabolomicsTools which is classified and searchable via a simple controlled vocabulary. CONCLUSION: This review presents the most widely used tools for metabolomics analysis, categorised based on their main functionality. As future work, we suggest a direct comparison of tools' abilities to perform specific data analysis tasks e.g. peak picking.

An ecophysiological and developmental perspective on variation in vessel diameter.

Variation in xylem vessel diameter is one of the most important parameters when evaluating plant water relations. This review provides a synthesis of the ecophysiological implications of variation in lumen diameter together with a summary of our current understanding of vessel development and its endogenous regulation. We analyzed inter-specific variation of the mean hydraulic vessel diameter (Dv ) across biomes, intra-specific variation of Dv under natural and controlled conditions, and intra-plant variation. We found that the Dv measured in young branches tends to stay below 30 µm in regions experiencing winter frost, whereas it is highly variable in the tropical rainforest. Within a plant, the widest vessels are often found in the trunk and in large roots; smaller diameters have been reported for leaves and small lateral roots. Dv varies in response to environmental factors and is not only a function of plant size. Despite the wealth of data on vessel diameter variation, the regulation of diameter is poorly understood. Polar auxin transport through the vascular cambium is a key regulator linking foliar and xylem development. Limited evidence suggests that auxin transport is also a determinant of vessel diameter. The role of auxin in cell expansion and in establishing longitudinal continuity during secondary growth deserve further study.

MetaboLights: An Open-Access Database Repository for Metabolomics Data.

MetaboLights is the first general purpose, open-access database repository for cross-platform and cross-species metabolomics research at the European Bioinformatics Institute (EMBL-EBI). Based upon the open-source ISA framework, MetaboLights provides Metabolomics Standard Initiative (MSI) compliant metadata and raw experimental data associated with metabolomics experiments. Users can upload their study datasets into the MetaboLights Repository. These studies are then automatically assigned a stable and unique identifier (e.g., MTBLS1) that can be used for publication reference. The MetaboLights Reference Layer associates metabolites with metabolomics studies in the archive and is extensively annotated with data fields such as structural and chemical information, NMR and MS spectra, target species, metabolic pathways, and reactions. The database is manually curated with no specific release schedules. MetaboLights is also recommended by journals for metabolomics data deposition. This unit provides a guide to using MetaboLights, downloading experimental data, and depositing metabolomics datasets using user-friendly submission tools.

Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport.

Stems that develop secondary vascular tissue (i.e. xylem and phloem derived from the vascular cambium) have unique demands on transport owing to their mass and longevity. Transport of water and assimilates must occur over long distances, while the increasing physical separation of xylem and phloem requires radial transport. Developing secondary tissue is itself a strong sink positioned between xylem and phloem along the entire length of the stem, and the integrity of these transport tissues must be maintained and protected for years if not decades. Parenchyma cells form an interconnected three-dimensional lattice throughout secondary xylem and phloem and perform critical roles in all of these tasks, yet our understanding of their physiology, the nature of their symplasmic connections, and their activity at the symplast-apoplast interface is very limited. This review highlights key historical work as well as current research on the structure and function of parenchyma in secondary vascular tissue in the hopes of spurring renewed interest in this area, which has important implications for whole-plant transport processes and resource partitioning.

Auxin-responsive DR5 promoter coupled with transport assays suggest separate but linked routes of auxin transport during woody stem development in Populus.

Polar auxin transport (PAT) is a major determinant of plant morphology and internal anatomy with important roles in vascular patterning, tropic growth responses, apical dominance and phyllotactic arrangement. Woody plants present a highly complex system of vascular development in which isolated bundles of xylem and phloem gradually unite to form concentric rings of conductive tissue. We generated several transgenic lines of hybrid poplar (Populus tremula x alba) with the auxin-responsive DR5 promoter driving GUS expression in order to visualize an auxin response during the establishment of secondary growth. Distinct GUS expression in the cambial zone and developing xylem-side derivatives supports the current view of this tissue as a major stream of basipetal PAT. However, we also found novel sites of GUS expression in the primary xylem parenchyma lining the outer perimeter of the pith. Strands of primary xylem parenchyma depart the stem as a leaf trace, and showed GUS expression as long as the leaves to which they were connected remained attached (i.e., until just prior to leaf abscission). Tissue composed of primary xylem parenchyma strands contained measurable levels of free indole-3-acetic acid (IAA) and showed basipetal transport of radiolabeled auxin ((3)H-IAA) that was both significantly faster than diffusion and highly sensitive to the PAT inhibitor NPA. Radiolabeled auxin was also able to move between the primary xylem parenchyma in the interior of the stem and the basipetal stream in the cambial zone, an exchange that was likely mediated by ray parenchyma cells. Our results suggest that (a) channeling of leaf-derived IAA first delineates isolated strands of pre-procambial tissue but then later shifts to include basipetal transport through the rapidly expanding xylem elements, and (b) the transition from primary to secondary vascular development is gradual, with an auxin response preceding the appearance of a unified and radially-organized vascular cambium.

Diversification and Expression of the PIN, AUX/LAX, and ABCB Families of Putative Auxin Transporters in Populus.

Intercellular transport of the plant hormone auxin is mediated by three families of membrane-bound protein carriers, with the PIN and ABCB families coding primarily for efflux proteins and the AUX/LAX family coding for influx proteins. In the last decade our understanding of gene and protein function for these transporters in Arabidopsis has expanded rapidly but very little is known about their role in woody plant development. Here we present a comprehensive account of all three families in the model woody species Populus, including chromosome distribution, protein structure, quantitative gene expression, and evolutionary relationships. The PIN and AUX/LAX gene families in Populus comprise 16 and 8 members respectively and show evidence for the retention of paralogs following a relatively recent whole genome duplication. There is also differential expression across tissues within many gene pairs. The ABCB family is previously undescribed in Populus and includes 20 members, showing a much deeper evolutionary history, including both tandem and whole genome duplication as well as probable gene loss. A striking number of these transporters are expressed in developing Populus stems and we suggest that evolutionary and structural relationships with known auxin transporters in Arabidopsis can point toward candidate genes for further study in Populus. This is especially important for the ABCBs, which is a large family and includes members in Arabidopsis that are able to transport other substrates in addition to auxin. Protein modeling, sequence alignment and expression data all point to ABCB1.1 as a likely auxin transport protein in Populus. Given that basipetal auxin flow through the cambial zone shapes the development of woody stems, it is important that we identify the full complement of genes involved in this process. This work should lay the foundation for studies targeting specific proteins for functional characterization and in situ localization.

Evolution of development of vascular cambia and secondary growth.

Secondary growth from vascular cambia results in radial, woody growth of stems. The innovation of secondary vascular development during plant evolution allowed the production of novel plant forms ranging from massive forest trees to flexible, woody lianas. We present examples of the extensive phylogenetic variation in secondary vascular growth and discuss current knowledge of genes that regulate the development of vascular cambia and woody tissues. From these foundations, we propose strategies for genomics-based research in the evolution of development, which is a next logical step in the study of secondary growth.

Effects of carbon dioxide and oxygen on sapwood respiration in five temperate tree species.

The gaseous environment surrounding parenchyma in woody tissue is low in O2 and high in CO2, but it is not known to what extent this affects respiration or might play a role in cell death during heartwood formation. Sapwood respiration was measured in two conifers and three angiosperms following equilibration to levels of O2 and CO2 common within stems, using both inner and outer sapwood to test for an effect of age. Across all species and tissue ages, lowering the O2 level from 10% to 5% (v/v) resulted in about a 25% decrease in respiration in the absence of CO2, but a non-significant decrease at 10% CO2. The inhibitory effect of 10% CO2 was smaller and only significant at 10% O2, where it reduced respiration by about 14%. Equilibration to a wider range of gas combinations in Pinus strobus L. showed the same effect: 10% CO2 inhibited respiration by about 15% at both 20% and 10% O2, but had no net effect at 5% O2. In an extreme treatment, 1% O2+20% CO2 increased respiration by over 30% relative to 1% O2 alone, suggesting a shift in metabolic response to high CO2 as O2 decreases. Although an increase in respiration would be detrimental under limiting O2, this extreme gas combination is unlikely to exist within most stems. Instead, moderate reductions in respiration under realistic O2 and CO2 levels suggest that within-stem gas composition does not severely limit respiration and is unlikely to cause the death of xylem parenchyma during heartwood formation.

Compression wood has little impact on the water relations of Douglas-fir (Pseudotsuga menziesii) seedlings despite a large effect on shoot hydraulic properties.

• Compression wood has been shown to reduce stem permeability, but it is not known to what extent it affects leaf-level processes. Here, we report whole-plant hydraulic properties of Douglas-fir (Pseudotsuga menziesii) seedlings induced to form varying amounts of compression wood. • Seedlings were grown under three bending treatments to assess the impact of compression wood on hydraulic properties, including stomatal conductance (gs ), above-ground shoot conductance (Kl(abg) ), and both specific and leaf area-specific conductivity (ks and kl , respectively). • Kl(abg) was significantly lower (50% reduction) in severely bent seedlings than in controls. Similarly, both ks and kl of the main axis were significantly reduced (by 52% and 46%, respectively) in severely bent seedlings relative to controls. Seedlings in the moderate bending treatments had ks and kl that were intermediate between controls and severe bending. • Despite clear differences in above-ground shoot hydraulic properties, severely bent seedlings maintained the same water potentials as controls and had similar diurnal patterns of gs . This suggests that when the entire soil-plant-atmosphere continuum is considered, even a severe reduction in stem ks caused by compression wood has little impact on leaf-level processes.

Hydraulic properties of Douglas-fir (Pseudotsuga menziesii) branches and branch halves with reference to compression wood.

Douglas-fir (Pseudotsuga menziesii var. menziesii (Mirb.) Franco) branch segments were used to test the hypothesis that compression wood reduces xylem transport efficiency. Whole 3-year-old segments were first measured for specific conductivity (k(s), m(2) s(-1) MPa(-1)), then split lengthwise into upper and lower halves, the latter containing all or most of the compression wood in the segment. Halves were then remeasured for k(s) using a new technique that prevents leakage of permeating fluid during measurements. Lower branch halves had significantly lower k(s) than upper halves (6.4 +/- 0.3 versus 9.3 +/- 0.3 m(2) s(-1) MPa(-1) x 10(-4), respectively; n = 36), and despite their larger size, significantly lower hydraulic conductivity (k(h), m(4) s(-1) MPa(-1)) than upper halves. Lower branch halves had higher specific gravity (0.51 +/- 0.01 versus 0.45 +/- 0.01; n = 36), lower water content (123 +/- 2% versus 155 +/- 3%; n = 36), and larger proportions of volume occupied by both cell wall and air than upper halves. Lower halves had more tracheids per annual ring than upper halves (73 +/- 3 versus 63 +/- 2 per radial transect, respectively; n = 36), but tracheids were shorter and had narrower lumens than those of upper branch halves. Differences in hydraulic properties between upper and lower halves suggest that compression wood does reduce xylem transport efficiency. In contrast, the amount of compression wood in each sample did not explain any variation in whole unsplit sample hydraulic properties.