Biology subjects

Kreiner, J. M.

Publications and source records attributed to Kreiner, J. M..

10 recordsLinked to original sources

bioRxiv2025

The genomic response to drought across spatiotemporal scales in Amaranthus tuberculatus

How genetic diversity responds to environmental change across spatiotemporal scales remains poorly understood despite its importance for species persistence in changing landscapes. Agricultural weeds offer ideal models for studying these adaptive dynamics as they rapidly evolve under both the intensive management practices designed to eliminate them and increasingly severe climate challenges such as drought. Here, we combine experimental and herbarium genomic approaches spanning within-generation to century-long timescales to understand how genome-wide variation responds to drought in Amaranthus tuberculatus. In this native species, a history of divergent selection between two ancestral lineages followed by secondary contact is thought to have facilitated its invasion into agriculture. A drought survival experiment on accessions from paired agricultural and natural populations across its range revealed substantial phenotypic variation differentiated by habitat, geography, and ancestry. Ancestry mapping revealed 43 independent regions across nearly all chromosomes that confer protective effects under drought, demonstrate particularly rapid allele frequency changes, and exhibit duration-specific selection over the course of the imposed drought. Observation of allele frequencies across the past century reveal evidence for climate-dependent fluctuating selection governing the evolution of drought-associated loci. Selection favors drought alleles during hot/dry years and selects against them in cool/wet years--a pattern more evident in long-term trends than in shorter temporal intervals, suggestive of adaptive lag in rapidly changing environments. By combining short and long-term spatiotemporal data, we demonstrate that fluctuating selection has preserved the polygenic variation underlying population responses to drought, enabling ongoing adaptive responses to contemporary land-use and climate change. Significance StatementUnderstanding how species cope with rapid climate and land use change requires studying evolutionary responses across scales. Using Amaranthus tuberculatus, a native species turned major agricultural weed, we bridge timescales by pairing a drought experiment with century-spanning herbarium genomics. We show that ancestry structures fitness under drought and has driven agricultural populations to be better drought-adapted. This involves many genes whose allele frequencies fluctuate with climate: drought-protective alleles increase during hot/dry years and decline in cool/wet years. These fluctuations maintain genetic diversity and enable climate tracking, which is imperfect over short timescales. By linking experimental and historical data, we uncover evolutionary dynamics missed by snapshots, improving predictions of species adaptation to environmental change and informing weed management.

evolutionary biology↗

bioRxiv2025

Rising temperatures favour parasite virulence and parallel molecular evolution following a host jump

Climate change is facilitating the poleward emergence of parasites, increasing the risk of jumping into new animal species, including humans. Whether more virulent or transmissible variants will spread during these climate-driven outbreaks is unclear. We experimentally evolved a wild parasitic bacterium, across the thermal range (20-30{degrees}C) and extremes (35{degrees}C) of Cape Verde - the site of field collection - in a novel, temperate animal host. At the parasites typical warm environmental temperature, we found that virulence escalated across evolutionary time. Parasites evolved at hot temperatures, towards the limit of host-parasite survival, displayed a cryptic virulence boost, deadlier once infecting animals at cooler temperatures. Patterns of molecular evolution were constrained to parallel changes in fewer loci at extreme temperatures. Our findings suggest that rising temperatures will leave predictable phenotypic and genomic signatures on evolving parasites as they emerge with climate change.

evolutionary biology↗

bioRxiv2024

The evolution, diversity, and genetic architecture of sex in waterhemp (Amaranthus tuberculatus)

The evolution of separate sexes is hypothesized to occur through distinct pathways involving few large-effect or many small-effect alleles. However, we lack empirical evidence for how these different genetic architectures shape the transition from quantitative variation in sex expression to distinct male and female phenotypes. To explore these processes, we leveraged the recent transition of Amaranthus tuberculatus to dioecy within a predominantly monoecious genus, along with a sex-phenotyped population genomic dataset, and six newly generated chromosome-level haplotype phased assemblies. We identify a [~]3 Mb region strongly associated with sex through complementary SNP genotype and sequence-depth based analyses. Comparative genomics of these proto-sex chromosomes within the species and across the Amaranthus genus demonstrates remarkable variability in their structure and genic content, including numerous polymorphic inversions. No such inversion underlies the extended linkage we observe associated with sex determination. Instead, we identify a complex presence/absence polymorphism reflecting substantial Y-haplotype variation--structured by ancestry, geography, and habitat-- but only partially explaining phenotyped sex. Just over 10% of sexed individuals show phenotype-genotype mismatch in the sex-linked region, and along with observation of leakiness in the phenotypic expression of sex, suggest additional modifiers of sex and dynamic gene content within and between the proto-X and Y. Together, this work reveals a complex genetic architecture of sex determination in A. tuberculatus characterized by the maintenance of substantial haplotype diversity, and variation in the expression of sex.

evolutionary biology↗

bioRxiv2023

Genome size and repeat content contribute to a complex architecture of flowering time in Amaranthus tuberculatus

Genome size variation, largely driven by repeat content, is poorly understood within and among populations, limiting our understanding of its significance for adaptation. Here we characterize intraspecific variation in genome size and repeat content across 186 individuals of Amaranthus tuberculatus, a ubiquitous native weed that shows flowering time adaptation to climate across its range and in response to agriculture. K-mer based genome size estimates vary by up to 20% across individuals, with transposable elements, unknown repeats, and rDNAs being the primary contributors to this variability. The additive effect of this variation has important phenotypic consequences--individuals with more repeats, and thus larger genomes, show slower flowering times and growth rates. Compared to newly-characterized gene copy number and polygenic nucleotide changes underlying variation in flowering time, we show that genome size remains a modest but significant contributor to the genetic basis of flowering time. Differences in flowering time across sexes and habitats are not mirrored by genome size variation, but rather polygenic variation and a gene copy number variant within the ATP synthesis pathway. Repeat content nonetheless shows non-neutral distributions across the genome, and across latitudinal and environmental gradients, reflecting numerous governing processes that in turn influence quantitative genetic variation for phenotypes key to plant adaptation. Author SummaryThe remarkable and seemingly inconsequential variation in genome size across species has long been an enigma in evolutionary biology. Calling this viewpoint into question, correlations between genome size variation and traits linked to fitness are increasingly uncovered. While this suggests that DNA content itself may be a source of adaptive genetic variation, repeat elements that propagate at the cost of the host are known to largely mediate this variation and may thus limit adaptive potential. Here we look to disentangle these multi-level dynamics, characterizing repeat dynamics across the genome and among individuals across diverse collections of a widespread agricultural weed, linking repeat content to genome size variation, and characterizing the relative importance of its phenotypic consequences. In Amaranthus tuberculatus, we find non-neutral repeat distributions across individuals across the range, and while this repeat variation underlies both variation in genome size and flowering time, we show that it makes a relatively minor contribution to variation in a fitness-related trait across the landscape relative to monogenic and polygenic features. Together, this work broadens our perspective on the complex selective dynamics that govern intraspecific variation in genome size and traits key to fitness in plants.

evolutionary biology↗

bioRxiv2022

Rapid adaptation and range expansion in response to agriculture over the last two centuries

North America has seen a massive increase in cropland use since 1800, accompanied more recently by the intensification of agricultural practices. Through genome analysis of present-day and historical samples spanning environments over the last two centuries, we studied the impact of these changes in farming on the extent and tempo of evolution across the native range of common waterhemp (Amaranthus tuberculatus), a now pervasive agricultural weed. Modern agriculture has imposed strengths of selection rarely observed in the wild, with striking shifts in allele frequency trajectories since agricultural intensification in the 1960s. An evolutionary response to this extreme selection was facilitated by a concurrent human-mediated range shift. By reshaping genome-wide diversity across the landscape, agriculture has driven the success of this weed in the 21st-century. One Sentence SummaryModern agriculture has shaped the evolution of a native plant into a weed by driving range shifts and strengths of selection rarely observed in the wild.

evolutionary biology↗

bioRxiv2021

Selective ancestral sorting and de novo evolution in the agricultural invasion of Amaranthus tuberculatus

The relative role of hybridization, de novo evolution, and standing variation in weed adaptation to agricultural environments is largely unknown. In Amaranthus tuberculatus, a widespread North American agricultural weed, adaptation is likely influenced by recent secondary contact and admixture of two previously isolated subspecies. We characterized the extent of adaptation and phenotypic differentiation accompanying the spread of A. tuberculatus into agricultural environments and the contribution of subspecies divergence. We generated phenotypic and whole-genome sequence data from a manipulative common garden experiment, using paired samples from natural and agricultural populations. We found strong latitudinal, longitudinal, and sex differentiation in phenotypes, and subtle differences among agricultural and natural environments that were further resolved with ancestry inference. The transition into agricultural environments has favoured southwestern var. rudis ancestry that leads to higher biomass and environment-specific phenotypes: increased biomass and earlier flowering under reduced water availability, and reduced plasticity in fitness-related traits. We also detected de novo adaptation to agricultural habitats independent of ancestry effects, including marginally higher biomass and later flowering in agricultural populations, and a time to germination home advantage. Therefore, the invasion of A. tuberculatus into agricultural environments has drawn on adaptive variation across multiple timescales--through both preadaptation via the preferential sorting of var. rudis ancestry and de novo local adaptation.

evolutionary biology↗

bioRxiv2021

Repeated origins, gene flow, and allelic interactions of herbicide resistance mutations in a widespread agricultural weed

Causal mutations and their frequency in agricultural fields are well-characterized for herbicide resistance. However, we still lack an understanding of their evolutionary history: the extent of parallelism in the origins of target-site resistance (TSR), how long these mutations persist, how quickly they spread, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of common waterhemp (Amaranthus tuberculatus), which we show to have undergone a massive expansion over the past century with a contemporary effective population size estimate of 8 x 107. We found variation at seven characterized TSR loci, two of which had multiple amino acid substitutions, and three of which were common. These three common resistance variants show parallelism in their mutational origins, with gene flow having shaped their distribution across the landscape. Allele age estimates supported a strong role of adaptation from de novo mutations, with a median allele age of 30 suggesting that most resistance alleles arose soon after the onset of herbicide use. However, resistant lineages varied in both their age and evidence for selection over two different timescales, implying considerable heterogeneity in the forces that govern their persistence. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We report a signal of extended haplotype competition between two common TSR alleles, and extreme linkage with genome-wide alleles with known functions in resistance adaptation. Together, this work reveals a remarkable example of spatial parallel evolution in a metapopulation, with important implications for the management of herbicide resistance.

evolutionary biology↗

bioRxiv2020

The genetic architecture and genomic context of glyphosate resistance

Much of what we know about the genetic basis of herbicide resistance has come from detailed investigations of monogenic adaptation at known target-sites, despite the increasingly recognized importance of polygenic resistance. Little work has been done to characterize the broader genomic basis of herbicide resistance, including the number and distribution of genes involved, their effect sizes, allele frequencies, and signatures of selection. In this work, we implemented genome-wide association (GWA) and population genomic approaches to examine the genetic architecture of glyphosate resistance in the problematic agricultural weed, Amaranthus tuberculatus. A GWA was able to correctly identify the gene targeted by glyphosate, but when we statistically controlled for two target-site genetic mechanisms, we found an additional 250 genes across all 16 chromosomes associated with non-target site resistance (NTSR). The encoded proteins had functions that have been linked to non-target site resistance (NTSR), the most significant of which is response to chemicals, but also showed pleiotropic roles in reproduction and growth. The architecture of NTSR was enriched for large effect sizes and low allele frequencies, suggesting the role of pleiotropic constraints on its evolution. The enrichment of rare alleles also suggested that the genetic architecture of NTSR may be population-specific and heterogeneous across the range. Despite their rarity, we found signals of recent positive selection on NTSR-alleles by both window- and haplotype-based statistics, and an enrichment of amino-acid changing variants. In our samples, genome-wide SNPs explain a comparable amount of the total variation in glyphosate resistance to monogenic mechanisms, even in a collection of individuals where 80% of resistant individuals have large-effect TSR mutations, indicating an underappreciated polygenic contribution to the evolution of herbicide resistance in weed populations.

evolutionary biology↗

bioRxiv2018

Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus

The selection pressure exerted by herbicides has led to the repeated evolution of herbicide resistance in weeds. The evolution of herbicide resistance on contemporary timescales in turn provides an outstanding opportunity to investigate key questions about the genetics of adaptation, in particular, the relative importance of adaptation from new mutations, standing genetic variation, or geographic spread of adaptive alleles through gene flow. Glyphosate-resistant Amaranthus tuberculatus poses one of the most significant threats to crop yields in the midwestern United States (1), with both agricultural populations and herbicide resistance only recently emerging in Canada (2, 3). To understand the evolutionary mechanisms driving the spread of resistance, we sequenced and assembled the A. tuberculatus genome and investigated the origins and population genomics of 163 resequenced glyphosate-resistant and susceptible individuals from Canada and the USA. In Canada, we discovered multiple modes of convergent evolution: in one locality, resistance appears to have evolved through introductions of preadapted US genotypes, while in another, there is evidence for the independent evolution of resistance on genomic backgrounds that are historically non-agricultural. Moreover, resistance on these local, non-agricultural backgrounds appears to have occurred predominantly through the partial sweep of a single haplotype. In contrast, resistant haplotypes arising from the midwestern US show multiple amplification haplotypes segregating both between and within populations. Therefore, while the remarkable species-wide diversity of A. tuberculatus has facilitated geographic parallel adaptation of glyphosate resistance, more recently established agricultural populations are limited to adaptation in a more mutation-limited framework.\n\nSignificanceWhile evolution is often thought of as playing out over millions of years, adaptation to new enviroments can occur in real time, presenting key opportunities to understand evolutionary processes. An important example comes from agriculture, where many weeds have evolved herbicide resistance. We have studied glyphosate resistant Amaranthus tuberculatus, a significant threat to crop yields in the midwestern US and Canada. Genome analyses showed that rapid evolution can either occur by \"borrowing\" resistance alleles from other locations, or by de novo evolution of herbicide resistance in a genetic background that was not previously associated with agriculture. Differences in recent evolutionary histories have thus favored either adaptation from pre-existing variation or new mutation in different parts of the A. tuberculatus range.

evolutionary biology↗

bioRxiv2017

Parental legacy, demography, and introgression influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae)

Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species and how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe and the Middle East. We phased the two subgenomes, one descended from the outcrossing and highly diverse Capsella grandiflora (Cg) and the other one from the selfing and genetically depauperate Capsella orientalis (Co). For each subgenome, we assessed its relationship with the diploid relatives, temporal change of effective population size Ne, signatures of positive and negative selection, and gene expression patterns. Introgression between C. bursa-pastoris and its diploid relatives was widespread and the two subgenomes were impacted differentially depending on geographic region. In all three regions, Ne of the two subgenomes decreased gradually and the Co subgenome accumulated more deleterious changes than Cg. Selective sweeps were more common on the Cg subgenome in Europe and the Middle East, and on the Co subgenome in Asia. In contrast, differences in expression were limited with the Cg subgenome slightly more expressed than Co in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence, the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy and were differentially affected by introgression and selection.

evolutionary biology↗