A bi‐organellar phylogenomic study of Pandanales: inference of higher‐order relationships and unusual rate‐variation patterns

We used a bi‐organellar phylogenomic approach to address higher‐order relationships in Pandanales, including the first molecular phylogenetic study of the panama‐hat family, Cyclanthaceae. Our genus‐level study of plastid and mitochondrial gene sets includes a comprehensive sampling of photosynthetic lineages across the order, and provides a framework for investigating clade ages, biogeographic hypotheses and organellar molecular evolution. Using multiple inference methods and both organellar genomes, we recovered mostly congruent and strongly supported relationships within and between families, including the placement of fully mycoheterotrophic Triuridaceae. Cyclanthaceae and Pandanaceae plastomes have slow substitution rates, contributing to weakly supported plastid‐based relationships in Cyclanthaceae. While generally slowly evolving, mitochondrial genomes exhibit sporadic rate elevation across the order. However, we infer well‐supported relationships even for slower evolving mitochondrial lineages in Cyclanthaceae. Clade age estimates across photosynthetic lineages are largely consistent with previous studies, are well correlated between the two organellar genomes (with slightly younger inferences from mitochondrial data), and support several biogeographic hypotheses. We show that rapidly evolving non‐photosynthetic lineages may bias age estimates upwards at neighbouring photosynthetic nodes, even using a relaxed clock model. Finally, we uncovered new genome structural variants in photosynthetic taxa at plastid inverted repeat boundaries that show promise as interfamilial phylogenetic markers.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/33/cla12417-sup-0025-TableS1.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/32/cla12417-sup-0017-FigS17.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/31/cla12417-sup-0004-FigS4.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/30/cla12417-sup-0019-FigS19.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/29/cla12417-sup-0020-FigS20.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/28/cla12417_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/27/cla12417-sup-0005-FigS5.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/26/cla12417-sup-0012-FigS12.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/25/cla12417-sup-0007-FigS7.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/24/cla12417-sup-0022-FigS22.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/23/cla12417-sup-0029-TableS5.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/22/cla12417-sup-0010-FigS10.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/21/cla12417-sup-0011-FigS11.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/20/cla12417-sup-0014-FigS14.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/19/cla12417-sup-0002-FigS2.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/18/cla12417-sup-0001-FigS1.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/17/cla12417.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/16/cla12417-sup-0030-TableS6.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/15/cla12417-sup-0021-FigS21.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/14/cla12417-sup-0023-FigS23.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/13/cla12417-sup-0009-FigS9.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/12/cla12417-sup-0031-TableS7.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/11/cla12417-sup-0006-FigS6.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/10/cla12417-sup-0003-FigS3.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/9/cla12417-sup-0024-FigS24.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/8/cla12417-sup-0008-FigS8.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/7/cla12417-sup-0028-TableS4.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/6/cla12417-sup-0016-FigS16.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/5/cla12417-sup-0013-FigS13.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/4/cla12417-sup-0018-FigS18.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/3/cla12417-sup-0026-TableS2.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/2/cla12417-sup-0015-FigS15.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162810/1/cla12417-sup-0027-TableS3.pd

Toward unifying global hotspots of wild and domesticated biodiversity

Global biodiversity hotspots are areas containing high levels of species richness, endemism and threat. Similarly, regions of agriculturally relevant diversity have been identified where many domesticated plants and animals originated, and co-occurred with their wild ancestors and relatives. The agro-biodiversity in these regions has, likewise, often been considered threatened. Biodiversity and agro-biodiversity hotspots partly overlap, but their geographic intricacies have rarely been investigated together. Here we review the history of these two concepts and explore their geographic relationship by analysing global distribution and human use data for all plants, and for major crops and associated wild relatives.We highlight a geographic continuum between agro-biodiversity hotspots that contain high richness in species that are intensively used and well known by humanity (i.e., major crops and most viewed species onWikipedia) and biodiversity hotspots encompassing species that are less heavily used and documented (i.e., crop wild relatives and species lacking information on Wikipedia). Our contribution highlights the key considerations needed for further developing a unifying concept of agro-biodiversity hotspots that encompasses multiple facets of diversity (including genetic and phylogenetic) and the linkage with overall biodiversity. This integration will ultimately enhance our understanding of the geography of human-plant interactions and help guide the preservation of nature and its contributions to people

Indigenous crop diversity maintained despite the introduction of major global crops in an African centre of agrobiodiversity

Societal Impact Statement The global success and expansion of a small pool of major crops, including rice, wheat and maize, risks homogenising global agriculture. Focusing on the agriculturally diverse Ethiopian Highlands, this study tested whether farm diversity tends to be lower among farmers who grow more introduced crops. Surprisingly, it was found that farmers have successfully integrated introduced crops, resulting in more diverse and heterogenous farms without negatively impacting indigenous crop diversity. This is encouraging because diverse farms, comprising indigenous agricultural systems supplemented by introduced crops, may help address global challenges such as food insecurity. Summary The global expansion of a handful of major crops risks eroding indigenous crop diversity and homogenising agroecosystems, with significant consequences for sustainable and resilient food systems. Here, we investigate the farm-scale impact of introduced crops on indigenous agroecosystems. We surveyed 1369 subsistence farms stratified across climate gradients in the Ethiopian Highlands, a hotspot of agrobiodiversity, to characterise the richness and cultivated area of the 83 edible crops they contained. We further categorise these crops as being indigenous to Ethiopia, or introduced across three different eras. We apply non-metric multidimensional scaling and mixed effects modelling to characterise agroecosystem composition across farms with different proportions of introduced crops. Crops from different periods do not differ significantly in frequency or abundance across farms. Among geographically matched pairs of farms, those with higher proportions of modern introduced crops had significantly higher overall crop richness. Furthermore, farms with a high proportion of modern introduced crops showed higher heterogeneity in crop composition. An analysis of socio-economic drivers indicated that poverty is negatively associated with the cultivated area of introduced crops. In our Ethiopian case study, global patterns of major crop expansion are not necessarily associated with agrobiodiversity loss at the farm scale or higher homogeneity across indigenous agricultural systems. Importantly, socioeconomic factors may influence farmers' propensity to adopt novel species, suggesting targets for agricultural extension policies. Given the rapid climatic, economic and demographic changes impacting global food systems and the threats to food security these entail, robust indigenous agricultural systems enriched with diverse introduced crops may help maintain resilience

Phylogenomic studies of the monocot sister orders Pandanales and Dioscoreales

The sister orders Pandanales and Dioscoreales are the last two major clades of monocots that remain to be examined in depth using phylogenomic approaches. Previous studies produced basic phylogenetic outlines for both orders, but left multiple higher-order relationships unresolved, including precise placements of non-photosynthetic mycoheterotrophic lineages. Species-level relationships in the Dioscorea yams, the largest Dioscoreales genus, are also poorly known despite the economic importance of this clade. Here I develop and apply phylogenomic methods to reconstruct the evolutionary histories of Pandanales, Dioscoreales and Dioscorea, using the resulting frameworks to address various phylogenetic and evolutionary hypotheses in each group. I employed a bi-organellar phylogenomic approach to resolve higher-order relationships in Pandanales, with mostly strong support. Mitogenomes are generally slowly evolving, but nevertheless permit inference of well-supported relationships. They also exhibit sporadic order-wide rate accelerations that are decoupled from plastome rate variation. I estimated clade ages to address several biogeographic hypotheses, and uncovered plastome structural variants that may define individual families. In Dioscoreales, I used plastid phylogenomic data and morphology to infer higher-order relationships. The molecular analyses resolve higher-order relationships, but are complicated by extreme substitution rate elevation observed in several mycoheterotrophic lineages. Nevertheless, my analyses confirm the non-monophyly of Burmanniaceae and Dioscoreaceae as currently circumscribed in angiosperm classification schemes. An updated morphological data set supports the local phylogenetic placement of several mycoheterotrophic genera for which plastid data are lacking, and ancestral-state reconstructions predict morphological synapomorphies relevant to the revision of family-level classification schemes. For phylogenomic studies of Dioscorea, I developed a customized bait panel comprising 260 low-to-single-copy nuclear genes. I assessed the utility of the panel with a pilot taxon sampling, supplemented with transcriptome data, that comprises representatives of all major Dioscorea clades, including multiple crop yams. The panel enables resolution of phylogenetic relationships at both deep and recent scales in Dioscorea, mostly with strong support, and provides insights into relationships between crop plants and putative crop wild relatives. Overall, my dissertation offers new insights into a broad diversity of evolutionary questions, made possible by resolution here of recalcitrant phylogenetic relationships in Pandanales, Dioscoreales and the Dioscorea yams.Science, Faculty ofBotany, Department ofGraduat

Plant agrodiversity to the rescue

Agricultural systems are vulnerable to climate change, and global reservoirs of plant genetic diversity are proving to be a valuable means of crop adaptation. A study now shows that production of sweet potato is at risk from extreme heat events, but a few tolerant cultivars can still thrive and potentially provide climate resilience

Afrothismiaceae (Dioscoreales), a new fully mycoheterotrophic family endemic to tropical Africa.

is a genus of non-photosynthetic mycoheterotrophs from the forests of continental tropical Africa. Multiple phylogenetic inferences using molecular data recover the genus as sister to a clade comprising mycoheterotrophic Thismiaceae and the photosynthetic family Taccaceae, contrary to earlier placements of and Thismiaceae within Burmanniaceae. Morphological support for separating from the rest of Thismiaceae has depended on the zygomorphic flowers of (although some species of are also zygomorphic), and their clusters of root tubers, each with a terminal rootlet. The number of described species of has recently increased from four to 16, with seven more species as yet undescribed; these discoveries have added morphological characters that support its distinction from Thismiaceae. Most notably, the ovary in has a single stalked placenta, and circumscissile fruits from which seeds are exserted by placental elevation (vs in Thismiaceae, three placentas, a deliquescing fruit lid, and seeds not exserted). stamens are inserted in the lower part of the floral tube, where they are attached to the stigma, and individual flowers are subtended by a single large dorsal bract. In contrast, in Thismiaceae, stamens are inserted at the mouth of the tube, free of and distant from the stigma, and each flower is subtended by a loose whorl of (2 –) 3 (– 4) bracts. Here we formally characterise Afrothismiaceae and review what is known of its development, seed germination, interactions with mycorrhizal Glomeromycota, biogeography, phylogeny and pollination biology. All but one ( ; Vulnerable) of the 13 species assessed on the IUCN Red List of Threatened Species are either Endangered or Critically Endangered; one species ( ) is considered extinct

A customized nuclear target enrichment approach for developing a phylogenomic baseline for Dioscorea yams (Dioscoreaceae)

Premise We developed a target enrichment panel for phylogenomic studies of Dioscorea, an economically important genus with incompletely resolved relationships. Methods Our bait panel comprises 260 low- to single-copy nuclear genes targeted to work in Dioscorea, assessed here using a preliminary taxon sampling that includes both distantly and closely related taxa, including several yam crops and potential crop wild relatives. We applied coalescent-based and maximum likelihood phylogenomic inference approaches to the pilot taxon set, incorporating new and published transcriptome data from additional species. Results The custom panel retrieved ~94% of targets and >80% of full gene length from 88% and 68% of samples, respectively. It has minimal gene overlap with existing panels designed for angiosperm-wide studies and generally recovers longer and more variable targets. Pilot phylogenomic analyses consistently resolve most deep and recent relationships with strong support across analyses and point to revised relationships between the crop species D. alata and candidate crop wild relatives. Discussion Our customized panel reliably retrieves targeted loci from Dioscorea, is informative for resolving relationships in denser samplings, and is suitable for refining our understanding of the independent origins of cultivated yam species; the panel likely has broader promise for phylogenomic studies across Dioscoreales

A customized nuclear target enrichment approach for developing a phylogenomic baseline for Dioscorea yams (Dioscoreaceae)

Premise We developed a target enrichment panel for phylogenomic studies of Dioscorea, an economically important genus with incompletely resolved relationships. Methods Our bait panel comprises 260 low- to single-copy nuclear genes targeted to work in Dioscorea, assessed here using a preliminary taxon sampling that includes both distantly and closely related taxa, including several yam crops and potential crop wild relatives. We applied coalescent-based and maximum likelihood phylogenomic inference approaches to the pilot taxon set, incorporating new and published transcriptome data from additional species. Results The custom panel retrieved ~94% of targets and >80% of full gene length from 88% and 68% of samples, respectively. It has minimal gene overlap with existing panels designed for angiosperm-wide studies and generally recovers longer and more variable targets. Pilot phylogenomic analyses consistently resolve most deep and recent relationships with strong support across analyses and point to revised relationships between the crop species D. alata and candidate crop wild relatives. Discussion Our customized panel reliably retrieves targeted loci from Dioscorea, is informative for resolving relationships in denser samplings, and is suitable for refining our understanding of the independent origins of cultivated yam species; the panel likely has broader promise for phylogenomic studies across Dioscoreales