Ecology

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Pollen collection and RNA extractionPollen is a microscopic and notoriously resistant plant product. Thus, methods to collect a sufficient and roughly equivalent volume of pollen per species, and to ensure RNA was collected from viruses both internal and external to pollen grains, were developed specifically for this work. At each of the four regions, we identified visually asymptomatic plants species that were in full flower and in high enough abundance to achieve our pollen sample minimum. Many of the pollen samples were collected from public roadsides. However, some from the California Grasslands were collected from the University of California’s McLaughlin Natural Reserve, and some from the Eastern Deciduous Agro-forest Interface were collected from the University of Pittsburgh’s Pymatuning Laboratory of Ecology. We had permission to sample in both places. In addition, we obtained permission from the USDA Forest Service to sample in the Till Ridge Cove area of the Chattahoochee-Oconee National Forest for sampling in Central Appalachia. None of the sampled plants displayed classic viral symptoms (e.g., leaf yellowing, vein clearing, leaf distortions, growth abnormalities). To achieve the broadest representation of plant species, we selected species in different families, where feasible. Also when possible, we focused primarily on perennial species to avoid any effects of life history variation. From these, we collected 30 to 50 mg of pollen from newly dehiscing anthers (3–967 fresh hermaphroditic flowers from 1–27 plants per species; Supplementary Table 3) in situ using a sterile sonic dismembrator (Fisherbrand Model 50, Fisher Scientific, Waltham, MA, USA) with a frequency of 20 Hz. We removed non-pollen tissues (e.g., anther debris) with sterile forceps. In addition to removing non-pollen debris that was visible to the naked eye in the field at the time of pollen sample collection, we conducted microscopic and gene expression analyses to confirm the purity of the pollen samples in the lab (Supplementary Methods). Visibly pure pollen from a single species was transferred to a 2-mL collection tube with Lysing Matrix D (MP Biomedicals, Irvine, CA, USA) and kept on dry ice until transported to and stored at −80°C at the University of Pittsburgh (Pittsburgh, PA, USA).Before extracting the total RNA, we freeze-dried the pollen samples (FreeZone 4.5 Liter Benchtop Freeze Dry System, Labconco Corporation, Kansas City, MO, USA) and lysed with a TissueLyser II (Qiagen, Inc., Germantown, MD, USA) at 30 Hz with varying times for different plant species (Supplementary Table 3). We confirmed via microscopy that this protocol resulted in the breakage of ≥50% of the pollen grains in a sample. The total RNA, including dsRNA, was extracted using the Quick-RNA Plant Miniprep Extraction Kit (Zymo Research Corporation, Irvine, CA, USA), following the full manufacturer’s protocol, including the optional steps of in-column DNA digestion and inhibitor removal.RNA sequencingWe assessed the quantity and quality of the total RNA extracted from each pollen sample with a Qubit 2.0 fluorometer (Invitrogen, ThermoFisher Scientific, Waltham, MA, USA) and with TapeStation analyses performed by the Genomics Research Core (GRC) at the University of Pittsburgh. Only samples with an RNA integrity value of ≥1.9 were used (Supplementary Table 3). Stranded RNA libraries were prepared by the GRC using the TruSeq Total RNA Library Kit (Illumina, Inc., San Diego, CA, USA), and ribosomal depletion was performed using a RiboZero Plant Leaf Kit (Illumina, Inc., San Diego, CA, USA). At the GRC, we pooled depleted RNA libraries from six species on a single lane of an Illumina NextSeq500 platform.Pre-virus detection stepsA sequencing depth of 117–260 million 75 bp paired-end reads was achieved per sample (Supplementary Table 3). Sequences were demultiplexed and trimmed of adapter sequences. We used the Pickaxe pipeline42,60,61 to detect known and novel pollen-associated viruses. First, Pickaxe removes poor-quality raw reads42,60,61 and aligns the quality-filtered reads using the Bowtie2 aligner with default parameters62 to a subtraction library. Each customized subtraction library contained the host plant species genome or the most closely related plant genomes in the National Center for Biotechnology Information (NCBI) database, if the host plant genome was not available (Supplementary Table 7), as well as other possible contaminant genomes (e.g., the human genome)42,60,61. The subtraction libraries with 1–8 closely related plant genomes, a bioinformatically tractable amount, were used to remove plant sequences, which allows for a conservative estimate of the viruses associated with pollen to be made. The size of the subtraction libraries did not influence the number of identified viruses, as there was no correlation between library size and either estimate of virus richness (conservative: r = 0.08, P = 0.75; relaxed: r = 0.06, P = 0.77). After subtraction, only non-plant reads remained and were used for viral detection.Known RNA virus detection, identity confirmationWith Pickaxe, we used the Bowtie2 aligner with default parameters62 (v2.3.4.2-3) to align viral non-plant reads to Viral RefSeq42,60,61 (hereafter, VRS; Index of /refseq/release/viral (nih.gov)). Each known virus reflects the top hit of an alignment to VRS42,60,61. Following Cantalupo et al.42, we considered a known virus to be present if the viral reads covered at least 20% of the top hit and aligned to it at least ten times. For viruses with segmented genomes, at least one segment was required to meet these criteria.Contig annotation and extension; novel RNA viral genome detection, identity confirmationViral reads were assembled into contigs using the CLC Assembly Cell (Qiagen Digital Insights, Redwood City, CA, USA), and Pickaxe was used to remove repetitive, short ( More

Female plants must not only allocate resources to flowering but also to producing seeds as well as fruits and/or cones. This suggests that the costs of reproduction are higher for female than male plants, or for female function of hermaphrodite plants. Some dioecious plants (i.e. separate male and female plants) are vegetatively very different (i.e. dimorphic) between the sexes, such as females having larger branch and leaf sizes. Differences between male and female resource allocation to reproduction and the possible consequences of this for vegetative dimorphism in dioecious plants, is a central issue in plant evolution but it is a controversial and difficult topic1,2. In the most highly cited paper on this topic, Obeso1 notes it is practically impossible to measure the direct costs of male and female allocation to sexual reproduction. For example, most vascular plant species (about 95%) are hermaphrodites which makes measuring direct allocation by the two sexes, difficult. Thus Paterno et al.3 used an indirect allometric method to measure sexual allocation in hermaphroditic inflorescences and concluded that larger flowers represent greater relative allocation to male function.The problem of shared sexual allocation to inflorescences is avoided in dioecious plants making them important tests for ideas of sexual allocation in plants. However, they are both rare as species and as individuals and are typically large, forest trees. For example, there are relatively few dioecious individual trees in the very large Barro Colorado forest tree data set4. Again, this large size makes direct measurement, such as of allocation to reproductive structures, difficult. The Cape Floral Region is a useful place to investigate sexual allocation in plants and its consequences, because dioecy is relatively common and vegetative dimorphism between the sexes can be extreme. Also, Cape plants are amenable to research being short (about 2–5 m), rapidly mature and short-lived (about 5–20 years). Thus, the large (about 85 spp.) Cape genus Leucadendron (Proteaceae) is probably the most researched genus globally for male and female differences5,6,7,8,9,10,11,12,13,14.Even in these dioecious plants it is difficult to directly measure allocation to male and female function because of the difficulty of finding a common currency to compare allocation. For example, comparing allocation differences in attractiveness, nectar, seeds, pollen, cones and fruits and differences in the timing of producing these structures1. In Leucadendron males are generally more visually attractive than females. This is achieved by the loss of photosynthetic capacity in floral leaves and bracts12,15. It would be difficult to directly compare this photosynthetic loss in males, with for instance, female allocation to cones and seeds. Despite the difficulties in directly measuring and comparing allocation to reproduction, the consensus is that female allocation to sexual reproduction typically exceeds male allocation1, including in Leucadendron2,9.Greater female allocation to reproduction is one of the suggested reasons for vegetative dimorphism between the sexes2. The three main hypotheses for sexual vegetative dimorphism are (i) greater female sexual resource allocation requires this to be balanced by having a more efficient physiology (resource use efficiency hypothesis), or (ii) greater female allocation requires females to be in the more optimum habitats (the sexual site dimorphism hypothesis) and this facilitates vegetative differences, such as larger female leaves in the more mesic habitats. Finally, (iii) vegetative dimorphism may be a consequence of selection on reproductive traits (reproductive traits hypothesis). In support of the resource use efficiency hypothesis in Leucadendron, Harris and Pannell9 argue that supplying water to live, closed cones in the canopy of serotinous Leucadendron females is a form of maternal care that non-serotinous species and males do not incur. To keep these cones from opening they need always to be hydrated and therefore serotinous females need to be more efficient in their water use than their males. They argued that fewer and thicker branches in females provides a hydraulic advantage. However, the data in Midgley8 and Roddy et al.14 showed no support for sexual differences in water use efficiency. Clearly, there are opposing views as to whether females allocate more to reproduction than males and whether females are eco-physiologically more efficient than males.The sexual site dimorphism hypothesis has not been tested for Leucadendron presumably because males and females co-occur on a small spatial scale16 but is tested in the present analysis of Aulax umbellata and A. cancellata. In support of the reproductive trait’s hypothesis, it was argued5 that in Leucadendron, vegetative dimorphism is an allometric consequence of selection for smaller male inflorescences. Smaller inflorescences are then associated with more, but narrower, stems and thus smaller leaves via Corners Rules5. Besides the evolutionary relevance for understanding sexual differences in allocation, it may also have conservation implications. For example, Hultine et al.17 argued that dioecious plants are under more threat than hermaphrodites because dioecious females are presumed to allocate more resources to reproduction than males. As global change progresses, females may suffer greater mortality and thus dioecious populations may have lower reproductive potential if they become more male biased.One way around the measurement problem of determining direct allocation to sexual reproduction is to use indirect methods based on trade-offs1 such as the influence of allocation to sexual reproduction, on sex ratios and sizes of co-occurring male and female plants. If for example, males allocated less to reproduction than co-occurring females, they should be relatively larger or live longer and this would impact size and sex ratios, especially as plants age and competition intensifies.
The Cape is uniquely suitable to consider allocation differences between the sexes because populations of dioecious Cape species are often large ( > 1000’s of plants ha−1) and with males and females co-existing at a fine spatial scale. The Cape Proteaceae grow in a stressful summer dry Mediterranean climate with nutrient-poor soils18. This provides strong selection on reproductive allocation to seeds (such as large size and high nutrient concentrations) to produce seedlings large enough to survive their first summer. The Cape Proteaceae are strongly fire-adapted. For example, many species are serotinous (canopy storage of seeds in live, closed cones which mainly open after fire)19. This too requires high female sex allocation to maintaining cones in the canopy. Most Cape Proteaceae species are post-fire re-seeders19 in that all plants die in fire. This results in single-aged populations of single-stemmed non-clonal individuals; adults die in fires and dense patches of seedlings establish in the first winter after the fire and die in the next fire. Co-occurring males and females have the same age and thus differences in size or sex ratios will mostly reflect allocation differences and competition rather than age or habitat. Also, because seedlings in the Cape grow up in an open post-fire environment, woody plants do not need to allocate specifically to height growth, to achieve full light. They are in full light their whole lives and therefore any sexual architectural differences do not reflect differences in habitat shadiness. Here we focused on Aulax umbellata, but also present sex ratios and size metrics for the congeneric A. cancellata. These are two common, single-stemmed strongly serotinous Cape species in the Proteaceae which are highly vegetatively dimorphic. Although both Leucadendron and Aulax are dioecious, a rare trait in the family, this represents independent evolution as the two genera are not close phylogenetically20. We test the hypothesis that vegetative sexual dimorphism in Aulax umbellata and Aulax cancellata can be explained by differences in allocation to growth. We predicted that co-occurring males and females would occur in equal sex ratios and be equal in size due to equal growth, despite vegetative dimorphism. More

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Department of Biology, McGill University, Montreal, Quebec, CanadaBrian Leung & Anna L. HargreavesBieler School of Environment, McGill University, Montreal, Quebec, CanadaBrian LeungDepartment of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, CanadaDan A. GreenbergSchool of Biology and Ecology and Mitchell Center for Sustainability Solutions, University of Maine, Orono, ME, USABrian McGillCentre for Biological Diversity, University of St Andrews, St Andrews, UKMaria DornelasIndicators and Assessments Unit, Institute of Zoology, Zoological Society of London, London, UKRobin FreemanB.L. wrote the response. A.C.H. and D.A.G. helped with writing, editing and discussing ideas. B.M. and M.D. discussed ideas with some editing. R.F. contributed discussions to the original manuscript2. More

Department of Biology, McGill University, Montreal, Quebec, CanadaBrian Leung & Anna L. HargreavesBieler School of Environment, McGill University, Montreal, Quebec, CanadaBrian LeungDepartment of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, CanadaDan A. GreenbergSchool of Biology and Ecology and Mitchell Center for Sustainability Solutions, University of Maine, Orono, ME, USABrian McGillCentre for Biological Diversity, University of St Andrews, St Andrews, UKMaria DornelasIndicators and Assessments Unit, Institute of Zoology, Zoological Society of London, London, UKRobin FreemanB.L. wrote the response. A.L.H. and D.A.G. helped with writing, editing and discussing ideas. B.M., M.D. and R.F. discussed ideas and did some editing. More

Cite this articleLeung, B., Hargreaves, A.L., Greenberg, D.A. et al. Reply to: Shifting baselines and biodiversity success stories.
Nature 601, E19 (2022). https://doi.org/10.1038/s41586-021-03749-zDownload citationPublished: 26 January 2022Issue Date: 27 January 2022DOI: https://doi.org/10.1038/s41586-021-03749-zShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard
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