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Loren H Rieseberg

Publications and source records attributed to Loren H Rieseberg.

12 recordsLinked to original sources

Predictive evolutionary genomics: principles, validation, and practice.

Climate change and habitat loss are driving rapid evolutionary responses in populations world-wide, which creates an urgent need for evolutionary forecasting in conservation and agriculture. Such forecasting can be categorized into three time scales: trait-based models that use multivariate quantitative genetic equations to project correlated phenotypic responses up to c. 20 generations, allele-based analyses that model allele frequency dynamics up to 100 generations, and composite adaptation scores that aggregate many small effects to yield predictions across longer horizons. However, these approaches have remained largely disconnected. Here, we present a Bayesian framework that integrates these three complementary approaches for evolutionary prediction. Our framework combines genomic, phenotypic, and environmental data to yield probabilistic predictions with explicit uncertainty. We show how predictive evolutionary forecasts can be validated with experimental evolution, field experimentation, historical specimens, and reciprocal transplants. These validated forecasts can help advance conservation and agricultural programmes by helping predict which populations are at risk of future extinction, optimizing breeding programmes for future climates, and planning ecosystem management under environmental change. By supporting a shift towards more predictive approaches in evolutionary biology, this framework may help improve our ability to manage biodiversity and food security in a changing world.

Genomics↗

Evolutionary Genomics Unravels the Responses and Adaptation to Climate Change in a Key Alpine Forest Tree Species.

Despite widespread biodiversity loss, our understanding of how species and populations will respond to accelerated climate change remains limited. In this study, we integrate population genomics, experimental evolution, and environmental modeling to elucidate the evolutionary responses to climate change in Populus lasiocarpa, a key alpine forest tree species primarily distributed in the mountainous regions of a global biodiversity hotspot. Over historical timescales, our findings demonstrate that demographic dynamics, divergent selection, and long-term balancing selection have shaped and maintained genetic variation within and between populations. In examining genomic signatures of contemporary climate adaptation, we found that haplotype blocks, potentially caused by inversion polymorphisms that suppress recombination, are linked to enriched combinations of locally adaptive environmental variations. We further assessed the relative contributions of environmentally induced plastic responses, constitutive expression divergence between genetic clusters, and their interactions in driving gene expression variation and divergence. Notably, we observed a strong correlation between sequence divergence and constitutive differential expression among genetic clusters. Finally, by incorporating genetic adaptation, migration, and genetic load into our predictions of population-level climate change risks, we identified western populations-primarily distributed in the Hengduan Mountains, a region known for its environmental heterogeneity and significant biodiversity-as the most vulnerable to climate change. These populations should be prioritized for conservation and management. Overall, our study advances the understanding of the relative roles of long-term natural selection, local environmental adaptation, and immediate plastic expression changes in shaping the responses of natural populations of keystone species to climate change.

Climate Change↗

The evolution of separate sexes in waterhemp is associated with surprising chromosomal diversity and complexity.

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.

Haplotypes↗

Major ecological transitions in wild sunflowers facilitated by hybridization.

Hybridization is frequent in many organismal groups, but its role in adaptation is poorly understood. In sunflowers, species found in the most extreme habitats are ancient hybrids, and new gene combinations generated by hybridization are speculated to have contributed to ecological divergence. This possibility was tested through phenotypic and genomic comparisons of ancient and synthetic hybrids. Most trait differences in ancient hybrids could be recreated by complementary gene action in synthetic hybrids and were favored by selection. The same combinations of parental chromosomal segments required to generate extreme phenotypes in synthetic hybrids also occurred in ancient hybrids. Thus, hybridization facilitated ecological divergence in sunflowers.

Adaptation, Physiological↗

The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations.

Segregating hybrids often exhibit phenotypes that are extreme or novel relative to the parental lines. This phenomenon is referred to as transgressive segregation, and it provides a mechanism by which hybridization might contribute to adaptive evolution. Genetic studies indicate that transgressive segregation typically results from recombination between parental taxa that possess quantitative trait loci (QTLs) with antagonistic effects (i.e. QTLs with effects that are in the opposite direction to parental differences for those traits). To assess whether this genetic architecture is common, we tabulated the direction of allelic effects for 3252 QTLs from 749 traits and 96 studies. Most traits (63.6%) had at least one antagonistic QTL, indicating that the genetic substrate for transgressive segregation is common. Plants had significantly more antagonistic QTLs than animals, which agrees with previous reports that transgressive segregation is more common in plants than in animals. Likewise, antagonistic QTLs were more frequent in intra- than in interspecific crosses and in morphological than in physiological traits. These results indicate that transgressive segregation provides a general mechanism for the production of extreme phenotypes at both above and below the species level and testify to the possible creative part of hybridization in adaptive evolution and speciation.

Adaptation, Physiological↗

Effects of genetic background on response to selection in experimental populations of Arabidopsis thaliana.

The extent to which genetic background can influence allelic fitness is poorly understood, despite having important evolutionary consequences. Using experimental populations of Arabidopsis thaliana and map-based population genetic data, we examined a multigeneration response to selection in populations with differentiated genetic backgrounds. Replicated experimental populations of A. thaliana with genetic backgrounds derived from ecotypes Landsberg and Niederzenz were subjected to strong viability and fertility selection by growing individuals from each population at high density for three generations in a growth chamber. Patterns of genome-wide selection were evaluated by examining deviations from expected frequencies of mapped molecular markers. Estimates of selection coefficients for individual genomic regions ranged from near 0 to 0.685. Genomic regions demonstrating the strongest response to selection most often were selected similarly in both genetic backgrounds. The selection response of several weakly selected regions, however, appeared to be sensitive to genetic background, but only one region showed evidence of positive selection in one background and negative selection in another. These results are most consistent with models of adaptive evolution in which allelic fitnesses are not strongly influenced by genetic background and only infrequently change in sign due to variation at other loci.

Arabidopsis↗

Directional selection is the primary cause of phenotypic diversification.

Selection is widely accepted as the principal force shaping phenotypic variation within populations. Its importance in speciation and macroevolution has been questioned, however, because phenotypic differences between species or higher taxa sometimes appear to be nonadaptive. Here, we use the quantitative trait locus (QTL) sign test to evaluate the importance of directional selection in phenotypic divergence. If a trait has a history of directional selection, QTL effects should be mostly in the same direction; otherwise QTLs with antagonistic effects should be common. Analysis of QTL effects for 572 traits from 86 studies revealed significantly fewer antagonistic QTLs than expected under neutrality, a result that validates Darwin's claim that phenotypic diversification is caused mainly by selection. Moreover, interspecific trait differences were more strongly or consistently selected than intraspecific differences, strengthening a growing consensus among students of speciation that directional selection is the primary cause of speciation. Contrary to studies of selection in contemporary populations, life history traits appear to be selected more strongly than morphological traits, but traits related to the timing of development are weakly selected relative to most other traits.

Animals↗

Genetic analysis of sunflower domestication.

Quantitative trait loci (QTL) controlling phenotypic differences between cultivated sunflower and its wild progenitor were investigated in an F(3) mapping population. Composite interval mapping revealed the presence of 78 QTL affecting the 18 quantitative traits of interest, with 2-10 QTL per trait. Each QTL explained 3.0-68.0% of the phenotypic variance, although only 4 (corresponding to 3 of 18 traits) had effects >25%. Overall, 51 of the 78 QTL produced phenotypic effects in the expected direction, and for 13 of 18 traits the majority of QTL had the expected effect. Despite being distributed across 15 of the 17 linkage groups, there was a substantial amount of clustering among QTL controlling different traits. In several cases, regions influencing multiple traits harbored QTL with antagonistic effects, producing a cultivar-like phenotype for some traits and a wild-like phenotype for others. On the basis of the directionality of QTL, strong directional selection for increased achene size appears to have played a central role in sunflower domestication. None of the other traits show similar evidence of selection. The occurrence of numerous wild alleles with cultivar-like effects, combined with the lack of major QTL, suggests that sunflower was readily domesticated.

Chromosome Mapping↗

Patterns of genetic variation suggest a single, ancient origin for the diploid hybrid species Helianthus paradoxus.

Experimental and comparative evidence implies that homoploid hybrid speciation is a reproducible process, mediated in part by ecological selection. Here, molecular data from the chloroplast genome and 17 nuclear microsatellite loci were employed to determine whether a well-documented homoploid hybrid species, Helianthus paradoxus, has arisen multiple times. Helianthus paradoxus is ecologically divergent from its parental species, and has a disjunct geographic distribution consistent with multiple origins. The molecular data, however, strongly support a single hybrid origin. First, all sampled populations of H. paradoxus are fixed for a single chloroplast DNA (cpDNA) haplotype, whereas local populations of both parental species, H. annuus and H. petiolaris, have multiple cpDNA haplotypes. Second, H. paradoxus populations form a single, well-supported clade (99.8% bootstrap support) in a neighbor-joining tree based on microsatellite allele frequencies. The microsatellite data also tentatively place the origin of H. paradoxus between 75,000 years and 208,000 years before present, indicating that anthropogenic disturbance likely did not play a role in the formation of this species. Finally, the genetic structure of this species is not consistent with passive riparian dispersal, which has been suggested for other wetland plant species, but may be explained by dispersal mechanisms implicated for H. annuus, such as large migratory mammals.

Alleles↗