Memoirs of a frequent flier: Phylogenomics reveals 18 long-distance dispersals between North America and South America in the popcorn flowers (Amsinckiinae).

PREMISE OF THE STUDY: American amphitropical disjunction (AAD) is an important but understudied New World biogeographic pattern in which related plants occur in extratropical North America and South America, but are absent in the intervening tropics. Subtribe Amsinckiinae (Boraginaceae) is one of the richest groups of plants displaying the AAD pattern. Here, we infer a time-calibrated molecular phylogeny of the group to evaluate the number, timing, and directionality of AAD events, which yields generalizable insights into the mechanism of AAD. METHODS: We perform a phylogenomic analysis of 139 samples of subtribe Amsinckiinae and infer divergence times using two calibration schemes: with only fossil calibrations and with fossils plus a secondary calibration from a recent family level analysis. Biogeographic analysis was performed in the R package BioGeoBEARS. KEY RESULTS: We document 18 examples of AAD in the Amsinckiinae. Inferred divergence times of these AAD examples were strongly asynchronous, ranging from Miocene (17.1 million years ago [Ma]) to Pleistocene (0.33 Ma), with most (12) occurring <5 Ma. Four events occurred 10-5 Ma, during the second rise of the Andes. All AAD examples had a North America to South America directionality. CONCLUSIONS: Second only to the hyperdiverse Poaceae in number of documented AAD examples, the Amsinckiinae is an ideal system for the study of AAD. Asynchronous divergence times support the hypothesis of long-distance dispersal by birds as the mechanism of AAD in the subtribe and more generally. Further comparative phylogenomic studies may permit biogeographic hypothesis testing and examination of the relationship between AAD and fruit morphology, reproductive biology, and ploidy.

Pleistocene radiation of the serpentine-adapted genus Hesperolinon and other divergence times in Linaceae (Malpighiales).

PREMISE OF THE STUDY: Hesperolinon (western flax; Linaceae) is endemic to the western United States, where it is notable for its high and geographically concentrated species diversity on serpentine-derived soils and for its use as a model system in disease ecology. We used a phylogenetic framework to test a long-standing hypothesis that Hesperolinon is a neoendemic radiation. METHODS: Five plastid and two ribosomal nuclear DNA gene regions were sampled from 105 populations of Hesperolinon, including all 13 recently recognized species across their known ranges. We used these data to generate population-level phylogenies of Hesperolinon. We also generated a robustly sampled chronogram of Linaceae using an eight-gene, 100-taxon supermatrix calibrated using fossil Linum pollen and a published chronogram of Malpighiales. KEY RESULTS: Most diversification in Hesperolinon has taken place in the past 1-2 million yr, much more recently than previous estimates. Only the earliest-diverging species, H. drymarioides, was resolved as a clade. Denser taxon and gene sampling generally support previously proposed relationships within Linaceae, but with more recent diversification of key clades. CONCLUSIONS: Hesperolinon is an excellent example of edaphic neoendemism, in support of Raven and Axelrod's hypothesis for the genus. Dense population-level sampling reveals a complex of incipient species, with clades poorly aligned with traditional morphological circumscriptions, likely due in part to continued gene flow. The diversification of Linaceae is more recent than previously estimated, and other recent radiations (e.g., Hugonia) warrant further study.

The reference genome of an endangered Asteraceae, Deinandra increscens subsp. villosa, endemic to the Central Coast of California.

We present a reference genome for the federally endangered Gaviota tarplant, Deinandra increscens subsp. villosa (Madiinae, Asteraceae), an annual herb endemic to the Central California coast. Generating PacBio HiFi, Oxford Nanopore Technologies, and Dovetail Omni-C data, we assembled a haploid consensus genome of 1.67 Gb as 28.7 K scaffolds with a scaffold N50 of 74.9 Mb. We annotated repeat content in 74.8% of the genome. Long terminal repeats (LTRs) covered 44.0% of the genome with Copia families predominant at 22.9% followed by Gypsy at 14.2%. Both Gypsy and Copia elements were common in ancestral peaks of LTRs, and the most abundant element was a Gypsy element containing nested Copia/Angela sequence similarity, reflecting a complex evolutionary history of repeat activity. Gene annotation produced 33,257 genes and 68,942 transcripts, of which 99% were functionally annotated. BUSCO scores for the annotated proteins were 96.0% complete of which 77.6% was single copy and 18.4% duplicates. Whole genome duplication synonymous mutation rates of Gaviota tarplant and sunflower (Helianthus annuus) shared peaks that correspond to the last Asteraceae polyploidization event and subsequent divergence from a common ancestor at ∼27 MYA. Regions of high-density tandem genes were identified, pointing to potentially important loci of environmental adaptation in this species.

Uncorrelated evolution of leaf and petal venation patterns across the angiosperm phylogeny.

Early angiosperm evolution, beginning approximately 140 million years ago, saw many innovations that enabled flowering plants to alter ecosystems globally. These included the development of novel, flower-based pollinator attraction mechanisms and the development of increased water transport capacity in stems and leaves. Vein length per area (VLA) of leaves increased nearly threefold in the first 30-40 million years of angiosperm evolution, increasing the capacity for transpiration and photosynthesis. In contrast to leaves, high water transport capacities in flowers may not be an advantage because flowers do not typically contribute to plant carbon gain. Although flowers of extant basal angiosperms are hydrated by the xylem, flowers of more recently derived lineages may be hydrated predominantly by the phloem. In the present study, we measured leaf and flower VLA for a phylogenetically diverse sample of 132 species from 52 angiosperm families to ask (i) whether flowers have lower VLA than leaves, (ii) whether flowers of basal angiosperm lineages have higher VLA than more recently derived lineages because of differences between xylem and phloem hydration, and (iii) whether flower and leaf VLA evolved independently. It was found that floral structures had lower VLA than leaves, but basal angiosperm flowers did not have higher VLA than more derived lineages. Furthermore, the independent evolution of leaf and petal VLA suggested that these organs may be developmentally modular. Unlike leaves, which have experienced strong selection for increased water transport capacity, flowers may have been shielded from such selective pressures by different developmental processes controlling VLA throughout the plant bauplan.

Conservation Genetics of the Endangered Lompoc Yerba Santa (Eriodictyon capitatum Eastw., Namaceae), including Phylogenomic Insights into the Evolution of Eriodictyon.

Eriodictyon capitatum (Namaceae) is a narrowly distributed shrub endemic to western Santa Barbara County, where it is known from only 10 extant California Natural Diversity Database element occurrences (EOs). Owing to low numbers of plants in nature, a limited overall extent, and multiple current threats, E. capitatum is listed as Endangered under the Federal Endangered Species Act and as Rare under the California Native Plant Protection Act. In the present study, high-throughput DNA sequence data were analyzed to investigate genetic diversity within and among all accessible EOs; to determine the extent of genetic isolation among EOs; to examine clonality within EOs; and to examine the taxonomic circumscriptions of E. capitatum, E. altissimum, E. angustifolium, and E. californicum through phylogenomic analysis. Population genetic analyses of E. capitatum reveal a pattern of strong genetic differentiation by location/EO. The clonality assessment shows that certain small EOs may support relatively few multilocus genotypes. The phylogenomic analyses strongly support the present-day taxonomic circumscriptions of both E. altissimum and E. capitatum, showing them to be reciprocally monophyletic and sister with strong support. Taken together, these results paint a picture of an evolutionarily and morphologically distinct species known from relatively few, genetically isolated stations.

Genetic and phenotypic diversity of Branchinecta sandiegonensis (Crustacea: Anostraca) in the vernal pools of Baja California, México.

Branchinecta sandiegonensis is a passively dispersed species that occurs in the vernal pool complexes of southern California, the USA, and northwestern Baja California, México. The fragmented distribution of these vernal pool complexes could limit the gene flow, generating high genetic structure and morphometric variation across the landscape. Here we estimate the genetic and phenotypic variation of B. sandiegonensis in the southern part of its range. We sampled 15 vernal pools from four geographic regions of the Baja California Peninsula. We genotyped 150 individuals using nuclear microsatellites and 31 individuals using the mitochondrial COI region. We also conducted a morphometric analysis on a sample of 232 individuals. We found moderate levels of genetic diversity and different patterns of structure depending upon the spatial scale of analysis. Demographic models suggest contrasting trends among populations. Phenotypically, we found high levels of heterogeneity in body size of fairy shrimps within and across the regions. Our findings highlight that vernal pools in Baja California are important reservoirs of genetic and phenotypic diversity for B. sandiegonensis. The interplay between gene flow and genetic drift may have influenced the patterns we detected in the southern part of the range of this species.

Monitoring within non-native ungulate exclosures documents the inherent size of Crocanthemum greenei (Cistaceae).

Crocanthemum greenei (B.L.Rob.) Sorrie (Cistaceae), a perennial sub-shrub, was measured as part of a demographic monitoring effort on Santa Catalina Island, California, USA (hereafter, Catalina). Introduced ungulate browsers remain present on Catalina. Consequently, many palatable plant taxa on the island are subject to and putatively limited by top-down browsing forces. Historically, introduced ungulates have also been present on each island throughout the range of Crocanthemum greenei. Habitat conservation work, resulting in the construction of ungulate exclosures on Catalina, has now allowed us to measure individuals in their mature, non-browsed form. The published value for Crocanthemum greenei stem (height) is usually 15-30 cm. While the original description hints at a greater potential size, recent descriptions appear to be influenced by observations made during the decades when plants would have been impacted by introduced ungulate herbivores. Here we present stem measurements of 81 adult individuals, with a median of 49 cm and an interquartile range of 42-56 cm. These measurements suggest an expanded stem (height) range of 15-60 cm better describes the taxon and shed light on the historical impacts of invasive ungulates across the islands and those continuing on Catalina.

Molecular and morphological evidence for recognition of two species within Harpagonella (Amsinckiinae, Boraginaceae).

Recent taxonomic treatments of the genus Harpagonella have included only one lower taxon, Harpagonella palmeri A. Gray. However, a larger-fruited variety of Harpagonella palmeri from Arizona and Sonora was described by I.M. Johnston in 1924. He continued to recognize this taxon - Harpagonella palmeri var. arizonica - in his treatment of the genus in Kearney and Peebles's Arizona Flora in 1960. Here, we provide two lines of molecular evidence and quantitative morphological evidence from calyx characters showing that plants of Harpagonella from Arizona, Sonora, and central Baja California, corresponding to Johnston's var. arizonica, are distinct from Harpagonella palmeri of southern California and Baja California. We make the new combination Harpagonella arizonica (I.M. Johnston) Guilliams & B.G. Baldwin, comb. nov. for the plants from Arizona, Sonora, and central Baja California.