Resurrected seeds from herbarium specimens reveal rapid evolution of drought resistance in a selfing annual.

PREMISE: Increased aridity and drought associated with climate change are exerting unprecedented selection pressures on plant populations. Whether populations can rapidly adapt, and which life history traits might confer increased fitness under drought, remain outstanding questions. METHODS: We utilized a resurrection ecology approach, leveraging dormant seeds from herbarium collections to assess whether populations of Plantago patagonica from the semi-arid Colorado Plateau have rapidly evolved in response to approximately ten years of intense drought in the region. We quantified multiple traits associated with drought escape and drought resistance and assessed the survival of ancestors and descendants under simulated drought. RESULTS: Descendant populations displayed a significant shift in resource allocation, in which they invested less in reproductive tissues and relatively more in both above- and below-ground vegetative tissues. Plants with greater leaf biomass survived longer under terminal drought; moreover, even after accounting for the effect of increased leaf biomass, descendant seedlings survived drought longer than their ancestors. CONCLUSIONS: Our results document rapid adaptive evolution in response to climate change in a selfing annual and suggest that shifts in tissue allocation strategies may underlie adaptive responses to drought in arid or semi-arid environments. This work also illustrates a novel approach, documenting that under specific circumstances, seeds from herbarium specimens may provide an untapped source of dormant propagules for future resurrection experiments.

Climate and the biotic community structure plant resistance across biogeographic groups of yellow monkeyflower.

Characterizing correlates of phytochemical resistance trait variation across a landscape can provide insight into the ecological factors that have shaped the evolution of resistance arsenals. Using field-collected data and a greenhouse common garden experiment, we assessed the relative influences of abiotic and biotic drivers of genetic-based defense trait variation across 41 yellow monkeyflower populations from western and eastern North America and the United Kingdom. Populations experience different climates, herbivore communities, and neighboring vegetative communities, and have distinct phytochemical resistance arsenals. Similarities in climate as well as herbivore and vegetative communities decline with increasing physical distance separating populations, and phytochemical resistance arsenal composition shows a similarly decreasing trend. Of the abiotic and biotic factors examined, temperature and the neighboring vegetation community had the strongest relative effects on resistance arsenal differentiation, whereas herbivore community composition and precipitation have relatively small effects. Rather than simply controlling for geographic proximity, we jointly assessed the relative strengths of both geographic and ecological variables on phytochemical arsenal compositional dissimilarity. Overall, our results illustrate how abiotic conditions and biotic interactions shape plant defense traits in natural populations.

Local adaptation of seed and seedling traits along a natural aridity gradient may both predict and constrain adaptive responses to climate change.

PREMISE: Variation in seed and seedling traits underlies how plants interact with their environment during establishment, a crucial life history stage. We quantified genetic-based variation in seed and seedling traits in populations of the annual plant Plantago patagonica across a natural aridity gradient, leveraging natural intraspecific variation to predict how populations might evolve in response to increasing aridity associated with climate change in the Southwestern U.S. METHODS: We quantified seed size, seed size variation, germination timing, and specific leaf area in a greenhouse common garden, and related these traits to the climates of source populations. We then conducted a terminal drought experiment to determine which traits were most predictive of survival under early-season drought. RESULTS: All traits showed evidence of clinal variation-seed size decreased, germination timing accelerated, and specific leaf area increased with increasing aridity. Populations with more variable historical precipitation regimes showed greater variation in seed size, suggestive of past selection shaping a diversified bet-hedging strategy mediated by seed size. Seedling height, achieved via larger seeds or earlier germination, was a significant predictor of survival under drought. CONCLUSIONS: We documented substantial interspecific trait variation as well as clinal variation in several important seed and seedling traits, yet these slopes were often opposite to predictions for how individual traits might confer drought tolerance. This work shows that plant populations may adapt to increasing aridity via correlated trait responses associated with alternative life history strategies, but that trade-offs might constrain adaptive responses in individual traits.

The strength of reproductive isolating barriers in seed plants: Insights from studies quantifying premating and postmating reproductive barriers over the past 15 years.

Speciation is driven by the evolution of reproductive isolating barriers that reduce, and ultimately prevent, substantial gene flow between lineages. Despite its central role in evolutionary biology, the process can be difficult to study because it proceeds differently among groups and may occur over long timescales. Due to this complexity, we typically rely on generalizations of empirical data to describe and understand the process. Previous reviews of reproductive isolation (RI) in flowering plants have suggested that prezygotic or extrinsic barriers generally have a stronger effect on reducing gene flow compared to postzygotic or intrinsic barriers. Past conclusions have rested on relatively few empirical estimates of RI; however, RI data have become increasingly abundant over the past 15 years. We analyzed data from recent studies quantifying multiple pre- and postmating barriers in plants and compared the strengths of isolating barriers across 89 taxa pairs using standardized RI metrics. Individual prezygotic barriers were on average stronger than individual postzygotic barriers, and the total strength of prezygotic RI was approximately twice that of postzygotic RI. These findings corroborate that ecological divergence and extrinsic factors, as opposed to solely the accumulation of genetic incompatibilities, are important to speciation and the maintenance of species boundaries in plants. Despite an emphasis in the literature on asymmetric postmating and postzygotic RI, we found that prezygotic barriers acted equally asymmetrically. Overall, substantial variability in the strengths of 12 isolating barriers highlights the great diversity of mechanisms that contribute to plant diversification.

Frequency-dependent fitness and reproductive dynamics contribute to habitat segregation in sympatric jewelflowers.

Coexistence results from a complex suite of past and contemporary processes including biogeographic history, adaptation, ecological interactions and reproductive dynamics. Here we explore drivers of local micro-parapatry in which two closely related and reproductively isolated Streptanthus species (jewelflower, Brassicaceae) inhabit continuous or adjacent habitat patches and occur within seed dispersal range, yet rarely overlap in fine-scale distribution. We find some evidence for abiotic niche partitioning and local adaptation, however differential survival across habitats cannot fully explain the scarcity of coexistence. Competition may also reduce the fitness of individuals migrating into occupied habitats, yet its effects are insufficient to drive competitive exclusion. Experimental migrants suffered reduced seed production and seed viability at sites occupied by heterospecifics, and we infer that heterospecific pollen transfer by shared pollinators contributes to wasted gametes when the two congeners come into contact. A minority disadvantage may reduce effective colonization of patches already occupied by heterospecifics, even when habitat patches are environmentally suitable. Differential adaptation and resource competition have often been evoked as primary drivers of habitat segregation in plants, yet negative reproductive interactions-including reproductive interference and decreased fecundity among low-frequency migrants-may also contribute to non-overlapping distributions of related species along local tension zones.

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.

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.