Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae)

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/141662/1/ajb20493.pd

Recent evolutionary divergence in a plant ring-species is not accompanied by floral phenology or pollinator shifts

Background and aims – The study of factors and processes involved in evolutionary divergence can inform how biodiversity is generated and maintained. We evaluate shifts in phenology or in pollination systems as potential barriers to gene exchange and thus promoters of divergence at the population-species boundary in the plant ring-species Euphorbia tithymaloides in the Caribbean. Material and methods – Combining collections-based and field-based observations and measurements, we evaluate evidence supporting that shifts in tempo of reproductive activity (floral phenology) or pollinator guilds (using visitation as a proxy) could be acting as mechanisms promoting divergence in E. tithymaloides. We focus on the geographic region where evolutionary divergence in this species has been documented: Greater and Lesser Antilles. Phenology data were derived from herbaria and online databases, for a total of 376 records across the Greater and Lesser Antilles. We quantified and characterized reward (nectar n = 13 sites) and gathered visitation data using direct observation (n = 12 sites) for a total of over 133 hours of observation/site. Key results – The peak of floral activity of E. tithymaloides is in winter, when days are short (~late October–late May). Under natural conditions, plants in the Antilles produce up to 22.4 µL of nectar, with mean sugar concentrations of ~ 46.5 ºBrix that amount to up to 10.3 mg of total sugars, with no significant differences observed between plants of the Lesser and Greater Antilles. Hummingbirds are the main floral visitors of E. tithymaloides in both areas: Greater Antilles: 61%, Lesser Antilles: 85%, and network analyses support a floral visitor community turnover across islands/countries. Conclusion – Evolutionary divergence in Caribbean E. tithymaloides along the Greater and Lesser Antilles is not accompanied by shifts in floral phenology or pollinator systems. Other factors, like pollinator turnover or pollinator-plant trait matching, might be at play. We outline hypotheses to this effect

Occupation of bare habitats, an evolutionary precursor to soil specialization in plants

Plant soil specialists contribute greatly to global diversity; however, the ecoevolutionary forces responsible for generating this diversity are poorly understood. We integrate molecular phylogenies with descriptive and experimental ecological data, creating a powerful framework with which to elucidate forces driving soil specialization. Hypotheses explaining edaphic specialization have historically focused on costs of adaptation to elements (e.g., nickel, calcium/magnesium) and accompanying tradeoffs in competitive ability in benign soils. We combine in situ microhabitat data for 37 streptanthoid species (Brassicaceae), soil analyses, and competition experiments with their phylogeny to reconstruct selective forces generating serpentine soil endemism, which has four to five independent origins in this group. Coupling ancestral state reconstruction with phylogenetic independent contrasts, we examine the magnitude and timing of changes in soil and habitat attributes relative to inferred shifts to serpentine. We find large changes in soil chemistry at nodes associated with soil shifts, suggesting that elemental changes occurred concomitantly with soil transitions. In contrast, the amount of bare ground surrounding plants in the field ("bareness"), which is greater in serpentine environments, is conserved across soil-type shifts. Thus, occupation of bare environments preceded shifts to serpentine, and may serve as an evolutionary precursor to harsh elemental soils and environments. In greenhouse experiments, taxa from barer environments are poorer competitors, a tradeoff that may contribute to soil endemism. The hypothesis of occupation of bare habitats as a precursor of soil specialization can be tested in other systems with a similar integrative ecophylogenetic approach, thereby providing deeper insights into this rich source of biodiversity

Single-copy nuclear gene primers for Streptanthus and other Brassicaceae from genomic scans, published data, and ESTs.

We report 11 primer sets for nine single-copy nuclear genes in Streptanthus and other Thelypodieae (Brassicaceae) and their utility at tribal-level and species-level phylogenetics in this poorly resolved group. • We selected regions based on a cross-referenced matrix of previous studies and public Brassica expressed sequence tags. To design primers, we used alignments of low-depth-coverage Illumina sequencing of genomic DNA for two species of Brassica mapped onto Arabidopsis thaliana. We report several primer combinations for five regions that consistently amplified a single band and yielded high-quality sequences for at least 70% of the species assayed, and for four additional regions whose utility might be clade specific. • Our primers will be useful in improving resolution at shallow depths across the Thelypodieae, and likely in other Brassicaceae

Macroevolutionary patterns of glucosinolate defense and tests of defense-escalation and resource availability hypotheses.

We explored macroevolutionary patterns of plant chemical defense in Streptanthus (Brassicaceae), tested for evolutionary escalation of defense, as predicted by Ehrlich and Raven's plant-herbivore coevolutionary arms-race hypothesis, and tested whether species inhabiting low-resource or harsh environments invest more in defense, as predicted by the resource availability hypothesis (RAH). We conducted phylogenetically explicit analyses using glucosinolate profiles, soil nutrient analyses, and microhabitat bareness estimates across 30 species of Streptanthus inhabiting varied environments and soils. We found weak to moderate phylogenetic signal in glucosinolate classes and no signal in total glucosinolate production; a trend toward evolutionary de-escalation in the numbers and diversity of glucosinolates, accompanied by an evolutionary increase in the proportion of aliphatic glucosinolates; some support for the RAH relative to soil macronutrients, but not relative to serpentine soil use; and that the number of glucosinolates increases with microhabitat bareness, which is associated with increased herbivory and drought. Weak phylogenetic signal in chemical defense has been observed in other plant systems. A more holistic approach incorporating other forms of defense might be necessary to confidently reject escalation of defense. That defense increases with microhabitat bareness supports the hypothesis that habitat bareness is an underappreciated selective force on plants in harsh environments

Macroevolutionary patterns of glucosinolate defense and tests of defense-escalation and resource availability hypotheses.

We explored macroevolutionary patterns of plant chemical defense in Streptanthus (Brassicaceae), tested for evolutionary escalation of defense, as predicted by Ehrlich and Raven's plant-herbivore coevolutionary arms-race hypothesis, and tested whether species inhabiting low-resource or harsh environments invest more in defense, as predicted by the resource availability hypothesis (RAH). We conducted phylogenetically explicit analyses using glucosinolate profiles, soil nutrient analyses, and microhabitat bareness estimates across 30 species of Streptanthus inhabiting varied environments and soils. We found weak to moderate phylogenetic signal in glucosinolate classes and no signal in total glucosinolate production; a trend toward evolutionary de-escalation in the numbers and diversity of glucosinolates, accompanied by an evolutionary increase in the proportion of aliphatic glucosinolates; some support for the RAH relative to soil macronutrients, but not relative to serpentine soil use; and that the number of glucosinolates increases with microhabitat bareness, which is associated with increased herbivory and drought. Weak phylogenetic signal in chemical defense has been observed in other plant systems. A more holistic approach incorporating other forms of defense might be necessary to confidently reject escalation of defense. That defense increases with microhabitat bareness supports the hypothesis that habitat bareness is an underappreciated selective force on plants in harsh environments