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Strauss, S. Y.

Publications and source records attributed to Strauss, S. Y..

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Greater benefits of assisted gene flow in F2 vs F1 progeny at the cold edge of a species' range

Gene flow to marginal populations at a species range edge can facilitate rapid adaptation by increasing genetic diversity, reducing inbreeding depression, and introducing novel alleles. In highly inbred populations, hybrid vigor is often observed in the first generation (F1), but hybrid breakdown may diminish fitness in subsequent generations. Thus, benefits of gene flow may be overestimated when only F1 performance is assessed. We tested whether gene flow among populations of the annual plant Erythranthe laciniata (A. Gray) G.L. Nesom, from similar and contrasting environments, confers persistent fitness advantages across F1 and F2 generations at the high-elevation edge of its range in the California Sierra Nevada. Gene flow was experimentally introduced through pollen transfer between cold-edge populations, between cold edge and central populations, and within local cold edge populations, and compared to self-fertilized offspring, the predominant mating strategy of E. laciniata. For F1 progeny, we measured morphological, phenological, and fitness traits in a common garden located near the cold-climate range limit during 2008-2009, a relatively average year, and for F2 progeny in 2009-2010, a relatively wet year. Although F1 crosses showed no initial performance advantage measured in the previous year, F2 progeny from center-to-edge and edge-to-edge crosses significantly outperformed selfed and locally outcrossed lines in fruit mass, total pedicels, biomass, and height. Our findings demonstrate that gene flow can confer long-term fitness benefits, especially among populations adapted to similar selective pressures, and highlight the potential of assisted gene flow to bolster or rescue peripheral populations facing climate change. SIGNIFICANCE STATEMENTSpecies living at the edges of their geographic ranges often have small, isolated populations with limited genetic diversity, which can restrict their ability to adapt to environmental change. Gene flow from other populations may increase adaptive potential, but its long-term consequences remain uncertain because most studies evaluate only first-generation hybrids. Using experimental crosses in the mountain wildflower Erythranthe laciniata, we show that gene flow can produce stronger fitness benefits in second-generation hybrids than in the first generation at a high-elevation range edge. These results suggest that recombination among populations can generate advantageous genetic combinations that emerge over multiple generations. Our findings highlight the potential for assisted gene flow to enhance adaptation and persistence of range-edge populations under climate change.

plant biology↗

Climate variability disrupts mutualism-driven increases in population persistence

Understanding how species interactions impact population dynamics and long-term persistence over broad temporal and spatial scales is crucial for predicting species distributions and responses to global change. Here, we integrate range-wide field surveys of [~]90 grass host populations spanning 13 years with demographic modeling based on six-year common garden experiments conducted across the host range to demonstrate that mutualistic fungal endophytes promote population-level persistence and growth of their native host grass across its distribution, with non-mutualistic populations four times more likely to go locally extinct. Despite providing population-level benefits, endophyte prevalence declined eight-fold more in historically mutualistic populations that experienced high climate variability. Thus, mutualisms can underpin population persistence and buffer hosts against environmental stress, but may themselves be vulnerable to global change, with concerning implications for long-term population viability and, ultimately, species distributions under an increasingly uncertain climate.

ecology↗

Herbarium specimens reveal a constrained seasonal climate niche despite diverged annual climates across a wildflower clade

Quantifying species niches across a clade reveals how environmental tolerances evolve, and offers insights into present and future distributions. We use herbarium specimens to explore climate niche evolution across 14 annual species of the Streptanthus (s.l.) clade (Brassicaceae), which originated in deserts and diversified into cooler, moister areas. To understand how climate niches evolved, we used historical climate records to estimate each species 1) classic annual climate niche, averaged over specimen collection sites; 2) growing season niche, from estimated specimen germination date to collection date, averaged across specimens (specimen-specific niche); and 3) standardized seasonal niche based on average growing seasons of all species (clade-seasonal niche). In addition to estimating how phenological variation maps onto climate niche evolution, we explored how spatial refugia shape the climate experienced by species by 1) analyzing how field soil texture changes relative to the climate space that species occupy and 2) comparing soil water holding capacity from each specimen locality to that of surrounding areas. Specimen-specific niches exhibited less clade-wide variation in climatic water deficit than did annual or clade-seasonal niches, and specimen-specific temperature niches showed no phylogenetic signal, in contrast to annual and clade-seasonal temperature niches. Species occupying cooler regions tracked hotter and drier climates by growing later into the summer, and by inhabiting refugia on drought-prone soils. These results underscore how phenological shifts, spatial refugia, and germination timing shape "lived" climate. Despite occupying a large range of annual climates, we found these species are constrained in the conditions under which they thrive. Significance statementHere, we show that closely related species that appear to have diverged in their climate niches based on highly differentiated annual conditions are actually tracking very similar seasonal climate conditions. This climate similarity, estimated from collection locations and associated weather data of nearly 2000 herbarium specimens, is achieved through the evolution of germination timing and plant flowering phenology, as well as establishment in spatial refugia with suitable microclimates. Our results highlight how occupation of a subset of seasonal conditions can be conserved across diverse species, resulting in less climate niche evolution than expected. Restricted climate niches imply that species may be less adaptable than we expect based on annual climates, and have implications for conservation, management and persistence under hotter climates.

ecology↗

Specimen-tailored "lived" climate reveals precipitation onset and amount best predict specimen phenology, but only weakly predict specimen reproductive success across a clade

Herbarium specimens are broadly distributed in space and time, enabling investigation of climate impacts on phenology and fitness. We reconstructed specimen "lived" climate from knowledge of germination cues and collection dates for 14 annual species in the Streptanthus (s.l.) clade (Brassicaceae) to ask: Which climate attributes, including the timing of precipitation onset, best explain specimen phenological stage and estimated reproduction? We also asked whether climate effects on phenology and reproduction were evolutionarily conserved. Precipitation amount and onset date, more than temperature, best predicted specimen phenology, but only weakly predicted reproduction. Earlier rainfall onset was associated with more phenologically advanced specimens, a relationship that showed phylogenetic signal. Few climate predictors explained variation in specimen reproduction. The lack of association between specimen reproduction and climate may arise from phenological shifts that buffer impacts of climate, interactions with other species, or challenges in estimating total reproduction from specimens. Our results highlight the value of specimen-tailored growing season conditions for reconstructing climate, incorporating evolutionary relationships in assessing responses to climate, and the complexities of estimating fitness from specimens. For the latter, we propose supplemental herbarium collections and community science protocols to increase the utility of these data for understanding climate impacts on populations.

ecology↗

Accelerated phenology fails to buffer fitness loss from delayed rain onset in a clade of wildflowers

The timing of early life cycle events has cascading effects on phenology and fitness. These effects may be critical for climate resilience of plant populations, especially in Mediterranean environments, where delayed rainfall onset causes delayed germination. To examine impacts of germination timing on ten species of the Streptanthus/Caulanthus clade, we induced germination across a range of dates in ambient seasonal conditions and recorded phenological and fitness traits. Later germination cohorts accelerated flowering, partially stabilizing flowering date, but the degree of this compensatory plasticity differed across species. Fitness declined with later germination; the magnitude of this decline depended on the balance between direct negative effects of later germination and compensatory positive effects of accelerated flowering. The resulting species differences in fitness responses suggest differential vulnerability to climate change. Species from wetter, cooler, less variable habitats accelerated flowering more and declined less in seed set with later germination, suggesting climate adaptation. However, other fitness responses to germination timing, like first year fitness, were evolutionarily labile across the clade and unrelated to climate. Although compensatory phenological plasticity may buffer the impacts of delayed germination, it cannot prevent long term declines in population fitness as fall rains come later with climate change.

evolutionary biology↗

A chromosome-level genome assembly of the varied leaved jewelflower, Streptanthus diversifolius, reveals a recent whole genome duplication

The Streptanthoid complex, a clade of primarily Streptanthus and Caulanthus genera in the Thelypodieae tribe (Brassicaceae) is an emerging model system for ecological and evolutionary studies. This Complex spans the full range of the California Floristic Province including desert, foothill, and mountain environments. The ability of these related species to radiate into dramatically different environments makes them a desirable study subject for exploring how plant species expand their ranges and adapt to new environments over time. Ecological and evolutionary studies for this complex have revealed fascinating variation in serpentine soil adaptation, defense compounds, germination, flowering, and life history strategies. Until now a lack of available genomic resources has hindered the ability to relate these phenotypic observations to their underlying genetic and molecular mechanisms. To help remedy this situation we present here a chromosome-level genome assembly of Streptanthus diversifolius, a member of the Streptanthoid Complex, developed using Illumina, Hi-C, and HiFi sequencing technologies. Construction of this assembly also provides further evidence to support the previously reported recent whole genome duplication unique to the Thelypodieae tribe. This whole genome duplication may have provided individuals in the Streptanthoid Complex the genetic arsenal to rapidly radiate throughout the California Floristic Province and to occupy commonly inhospitable environments including serpentine soils.

genomics↗

Germination responses to experimental rainfall timing identify potential vulnerability to climate change across a clade of California wildflowers

The timing of germination, driven by seasonal cues, is critical for the life cycle of plants. Variation among species in germination responses can reflect evolutionary processes and adaptation to local climate and can affect vulnerability to changing conditions. Indeed, climate change is altering the timing of precipitation and associated temperatures, which may interact with germination cueing to affect the timing, quantity, and speed of germination. Germination responses to change can then have consequences for individual fitness, population dynamics, and species distributions. Here, we assessed responses to the timing of germination-triggering rains and corresponding temperatures for 11 species spanning the Streptanthus (s.l.) clade (Brassicaceae). To do so, we experimentally manipulated the onset date of rainfall events, measured effects on germination fraction and rate, and evaluated whether responses were constrained by evolutionary relationships across the phylogeny. We then explored the possible consequences of these responses to contemporary shifts in precipitation timing. Later onset rains and cooler temperatures significantly reduced germination rates for all species. Germination fractions decreased with later rains and cooler temperatures for all but three Caulanthus species. Species germination responses to the timing of rainfall and seasonal temperatures were phylogenetically constrained, with Caulanthus species appearing less sensitive. Further, six species are likely already experiencing significant decreases in germination fractions or rates (or both) with observed climate change, which has shifted the timing of rainfall towards the cooler, winter months in California. Overall, our findings highlight the importance of the germination responses to seasonal timing, how they have evolved across the clade, and their implications under climate change.

plant biology↗

Plant species within Streptanthoid Complex associate with distinct microbial communities that shift to be more similar under drought

Prolonged water stress can reduce plant growth and fitness and may shift rhizoplane microbial communities. Although drought affects microbial structure of many plant species, it is still poorly understood whether closely related plant species host distinct microbial communities or respond similarly to drought. To explore this question, eight members of the Streptanthus clade with varying affinity to serpentine were subjected to three watering regimes. Rhizoplane bacterial communities were described using 16S rRNA gene amplicon sequencing and we explored the impact of watering treatment and plant species on alpha diversity, differential abundance, and beta diversity of soil bacterial communities. Among most plant species, reduced watering also reduced alpha diversity, but plant species did not strongly impact alpha diversity. Drought treatment reduced microbial community dissimilarity among samples: bacterial communities were more similar when plants received less water. Watering altered the relative abundance of bacterial genera within Proteobacteria, Firmicutes, Bacteroidetes, Planctomycetes, and Acidobacteria, which responded similarly in the rhizoplane of most plant species. These results suggest that prolonged water stress in Streptanthus spp. can result in convergent microbial communities among plant species. We suggest the functional consequences of these shifts be examined to assess effects on plant and microbial fitness under drought conditions.

genomics↗

Strengthened mutualistic adaptation between teosinte and its rhizosphere biota in cold climates

O_LIWhile abiotic environments consistently shape local adaptation, the strength of local adaptation to biotic interactions may vary more. One theory, COCO (CO-evolutionary Outcomes across Conditionality), predicts it may be strongest where species experience greater stress, because stress increases fitness impacts of species interactions. For example, in plant interactions with rhizosphere biota, positive outcomes increase with stress from low soil fertility, drought and cold. C_LIO_LITo investigate the influence of abiotic stress gradients on adaptation between plants and rhizosphere biota, we used a greenhouse common garden experiment recombining teosinte, Zea mays ssp. mexicana (wild relative of maize), and rhizosphere biota, collected across a stress gradient (elevational variation in temperature, precipitation, and nutrients). C_LIO_LIWe found stronger local adaptation between teosinte and rhizosphere biota from colder, more stressful sites, as expected by COCO. However, biota from less stressful, warmer sites provided greater average benefits across teosinte populations. Links between plant traits and 20-element profiles of plant leaves explained fitness variation, persisted in the field, were influenced by both plants and biota, and largely reflected patterns of local adaptation. C_LIO_LIIn sum, we uncovered greater local adaptation to biotic interactions in colder sites, and that both plants and rhizosphere biota affect the expression of plant phenotypes. C_LI

evolutionary biology↗

Adaptive phenotypic divergence in teosinte differs across biotic contexts

Climate is a powerful force shaping adaptation within species, often creating dramatic phenotypic clines. Yet adaptation to climate does not occur in a vacuum: species interactions filter the fitness consequences of both climatic and phenotypic variation. In other words, the translation of genotype to phenotype may be altered by biotic context, influencing the variation upon which climatic selection can act. We investigate the role of such interactions in changing the phenotypes on which selection acts using ten populations of an annual grass species (teosinte: Zea mays ssp. mexicana) sourced from along an elevational gradient, along with rhizosphere biota sourced from three of those populations. We grow teosinte families in a half-sibling design in separate biota treatments to first test whether the divergence we see among traits in teosinte populations exceeds what we would expect from genetic drift and then whether the source of rhizosphere biota affects the expression of divergent traits. We also assay the influence of these three rhizosphere biotas on contemporary additive genetic variation in teosinte traits across populations. We find that expression of most measured traits in teosinte is altered by rhizosphere biota, as well as the degree of variance and covariance among traits involved in root mass and flowering time. As a number of these traits are also found to underlie adaptive divergence across habitats, our data suggest that biota influence the expression of traits underlying local adaptation. Together, our results suggest that changes in trait expression and covariance elicited by interactor communities in root mass and flowering time may have played a historical role in local adaption of teosinte to environments, and that they would play a contemporary role in responses to changing selection pressures.

evolutionary biology↗