Genome size evolution is associated with climate seasonality and glucosinolates,but not life history,soil nutrients or range size,across a clade of mustards

Background and AimsWe investigate patterns of evolution of genome size across a morphologically and ecologically diverse clade of Brassicaceae, in relation to ecological and life history traits. While numerous hypotheses have been put forward regarding autecological and environmental factors that could favour small vs. large genomes, a challenge in understanding genome size evolution in plants is that many hypothesized selective agents are intercorrelated.MethodsWe contribute genome size estimates for 47 species of Streptanthus Nutt. and close relatives, and take advantage of many data collections for this group to assemble data on climate, life history, soil affinity and composition, geographic range and plant secondary chemistry to identify simultaneous correlates of variation in genome size in an evolutionary framework. We assess models of evolution across clades and use phylogenetically informed analyses as well as model selection and information criteria approaches to identify variables that can best explain genome size variation in this clade.Key ResultsWe find differences in genome size and heterogeneity in its rate of evolution across subclades of Streptanthus and close relatives. We show that clade-wide genome size is positively associated with climate seasonality and glucosinolate compounds. Model selection and information criteria approaches identify a best model that includes temperature seasonality and fraction of aliphatic glucosinolates, suggesting a possible role for genome size in climatic adaptation or a role for biotic interactions in shaping the evolution of genome size. We find no evidence supporting hypotheses of life history, range size or soil nutrients as forces shaping genome size in this system.ConclusionsOur findings suggest climate seasonality and biotic interactions as potential forces shaping the evolution of genome size and highlight the importance of evaluating multiple factors in the context of phylogeny to understand the effect of possible selective agents on genome size.     

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers

Speciation occurs when reproductive barriers substantially reduce gene flow between lineages. Understanding how specific barriers contribute to reproductive isolation offers insight into the initial forces driving divergence and the evolutionary and ecological processes responsible for maintaining diversity. Here, we quantified multiple pre‐ and post‐pollination isolating barriers in a pair of closely related California Jewelflowers (Streptanthus, Brassicaceae) living in an area of sympatry. S. breweri and S. hesperidis are restricted to similar serpentine habitats; however, populations are spatially isolated at fine‐scales and rarely co‐occur in intermixed stands. Several intrinsic postzygotic barriers were among the strongest we quantified, yet, postzygotic barriers currently contribute little to overall reproductive isolation due to the cumulative strength of earlier‐acting extrinsic barriers, including spatial isolation, and flowering time and pollinator differences. Data from multiple years suggest that pre‐pollination barriers may have different strengths depending on annual environmental conditions. Similarly, crossing data suggest that the strength of intrinsic isolation may vary among different population pairs. Estimates of total reproductive isolation in S. breweri and S. hesperidis are robust to uncertainty and variability in individual barrier strength estimates, demonstrating how multiple barriers can act redundantly to prevent gene flow between close relatives living in sympatry.     

A comparative genomic map for Caulanthus amplexicaulis and related species (Brassicaceae)

Adaptation to environment is the cornerstone of ecological genetics. The subject of this study is a wild relative of the sequenced and annotated model plant species, Arabidopsis thaliana. Caulanthus amplexicaulis var. barbarae lives on serpentine soils, known for high concentrations of heavy metals and low concentrations of essential plant macronutrients, and provides a compelling example of an organism’s adaptation to environment. We constructed an F₂ linkage map, using a cross to the nonserpentine sister taxon, C. amplexicaulis var. amplexicaulis. C. amplexicaulis is a member of a highly diverse set of taxa (within the tribe Thelypodieae), described here as the ‘Streptanthoid Complex’ that are adapted to a broad range of environments, yet share a common n = 14 chromosome number and likely arose by a recent radiation. The linkage map consists of 97 polymorphic microsatellite markers, and 40 exon‐primed intron‐crossing markers based on A. thaliana exon sequences and Brassica ESTs. The map covers 14 linkage groups and has a total length of 1513 cM. Both the patterns of marker segregation and the comparative map indicate that C. amplexicaulis is a diploid organism with a compact genome. All exon‐primed intron‐crossing markers, and an unexpectedly large number of microsatellite markers (83%), had significant similarity to the A. thaliana genome, facilitating the development of a comparative genome map. As a proof of principle, we used the comparative map to identify candidate genes underlying differences in sepal colour between the two parent taxa. We demonstrate that the genomic tools developed here will be portable throughout the Streptanthoid Complex.     

The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator

Background: The flora of serpentine/ultramafic soils provides an excellent model system for the study of natural selection in plant populations. Streptanthus polygaloides is a nickel hyperaccumulator that is endemic to serpentine soils in the Sierra Nevada of California, and has four floral morphs (yellow, purple, yellow-to-purple and undulate).

Aims: We investigate three hypotheses: (1) the purple morph occurs in colder, wetter climates than the yellow morph; (2) tissue–soil ionic relationships differ among morphs; and (3) morphs occur on soils with differing elemental concentrations.

Methods: We queried herbarium records to investigate patterns of occurrence among the yellow and purple floral morphs, and analysed soil and tissue samples from wild populations of all four morphs.

Results: The purple morph inhabited serpentine outcrops with colder temperatures and greater precipitation levels than the yellow morph. Concentrations of elements in leaf tissue and rhizosphere soil differed little among populations of the morphs, but showed substantial within-site variation.

Conclusions: Our results suggest that a climatic gradient may be responsible for divergence in floral colour among populations of S. polygaloides. Because of the large within-site variation in soil and tissue elemental concentrations, plants appear to have a varied physiological response to edaphic factors, regardless of morph membership.     

Along the speciation continuum: Quantifying intrinsic and extrinsic isolating barriers across five million years of evolutionary divergence in California jewelflowers

Understanding the relative roles of intrinsic and extrinsic reproductive barriers, and their interplay within the geographic context of diverging taxa, remains an outstanding challenge in the study of speciation. We conducted a comparative analysis of reproductive isolation in California Jewelflowers (Streptanthus, s.l., Brassicaceae) by quantifying potential barriers to gene flow at multiple life history stages in 39 species pairs spanning five million years of evolutionary divergence. We quantified nine potential pre‐ and postzygotic barriers and explored patterns of reproductive isolation in relation to genetic distance. Intrinsic postzygotic isolation was initially weak, increased at intermediate genetic distances, and reached a threshold characterized by complete genetic incompatibility. Climatic niche differences were strong at shallow genetic distances, and species pairs with overlapping ranges showed slight but appreciable phenological isolation, highlighting the potential for ecological barriers to contribute to speciation. Geographic analyses suggest that speciation is not regionally allopatric in the California Jewelflowers, as recently diverged taxa occur in relatively close proximity and display substantial range overlap. Young pairs are characterized by incomplete intrinsic postzygotic isolation, suggesting that extrinsic barriers or fine‐scale spatial segregation are more important early in the divergence process than genetic incompatibilities.     

Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae)

Plants use chemical defences to reduce damage from herbivores and the effectiveness of these defences can be altered by biotic and abiotic factors, such as herbivory and soil resource availability. Streptanthus polygaloides , a nickel (Ni) hyperaccumulator, possesses both Ni-based defences and organic defences (glucosinolates), but the extent to which these defences interact and respond to environmental conditions is unknown. S. polygaloides plants were grown on high-Ni and low-Ni soil and concentrations of Ni and glucosinolates were compared with those of the congeneric non-hyperaccumulator, S. insignus spp. insignus , grown under the same conditions. Ni contents were highest (4000 μg g⁻¹ dry tissue) in S. polygaloides plants grown on high-Ni soil. Glucosinolate content was significantly higher in S. insignus than in S. polygaloides suggesting that plants defended by Ni produce a lower concentration of organic defences. In a separate experiment, high-Ni S. polygaloides plants were exposed to simulated herbivory or live folivores to determine the inducibility of Ni-based and organic defences. Contents of Ni were not affected by either herbivory treatment, whereas glucosinolate concentrations were >30% higher in damaged plants. We concluded that the Ni-based defence of S. polygaloides is not induced by herbivory.     

Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode

No study of a single nickel (Ni) hyperaccumulator species has investigated the impact of hyperaccumulation on herbivores representing a variety of feeding modes. Streptanthus polygaloides plants were grown on high- or low-Ni soils and a series of no-choice and choice feeding experiments was conducted using eight arthropod herbivores. Herbivores used were two leaf-chewing folivores (the grasshopper Melanoplus femurrubrum and the lepidopteran Evergestis rimosalis), a dipteran rhizovore (the cabbage maggot Delia radicum), a xylem-feeder (the spittlebug Philaenus spumarius), two phloem-feeders (the aphid, Lipaphis erysimi and the spidermite Trialeurodes vaporariorum) and two cell-disruptors (the bug Lygus lineolaris and the whitefly Tetranychus urticae). Hyperaccumulated Ni significantly decreased survival of the leaf-chewers and rhizovore, and significantly reduced population growth of the whitefly cell-disruptor. However, vascular tissue-feeding insects were unaffected by hyperaccumulated Ni, as was the bug cell-disruptor. We conclude that Ni can defend against tissue-chewing herbivores but is ineffective against vascular tissue-feeding herbivores. The effects of Ni on cell-disruptors varies, as a result of either variation of insect Ni sensitivity or the location of Ni in S. polygaloides cells and tissues.     

Primers for 10 polymorphic microsatellites from Caulanthus amplexicaulis var. barbarae,and cross‐amplification in other species within the Streptanthoid Complex (Brassicaceae)

Ten microsatellite primer pairs, developed from Caulanthus amplexicaulis var. barbarae (J. Howell) Munz, specifically amplified target loci across a diverse range of taxa from the Streptanthoid Complex, Brassicaceae. All primer pairs produced amplification products from at least 22 of the 23 accessions tested. Product size variation and observable heterozygosity were consistent with what would be expected from the amplification of polymorphic microsatellites across the complex. Our findings demonstrate that microsatellites developed for C. amplexicaulis var. barbarae will be useful for population‐genetic studies in taxa throughout the Streptanthoid Complex.