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Eaton, D. A. R.

Publications and source records attributed to Eaton, D. A. R..

11 recordsLinked to original sources

Organelle Capture, Lineage-Specific Genomic Responses, and the Lability of Dioecy in Amaranthus

The transition from combined to separate sexes in plants drives genomic change, from recombination suppression at sex-determining loci to shifts in selection across autosomes and cytoplasmic genomes. In Amaranthus, a genus that includes ancient grain crops and noxious weeds, separate sexes arose twice through non-homologous sex-determining architectures, with at least one reversion to monoecy, yet plastid and mitochondrial phylogenies group the two dioecious lineages together despite independent origins. The source of this discordance and whether independent origins of dioecy produced parallel or lineage-specific genomic responses remain unknown. We sampled nuclear, plastid, and mitochondrial genomes across 19 species, resolving the backbone phylogeny of the genus and dating the crown to 2-5 Ma. Coalescent simulations rejected incomplete lineage sorting in favor of multiple organelle capture events, implying historical exchange across reproductive barriers separating the two dioecious clades. Nuclear allele sharing was concentrated within each dioecious clade rather than between them, consistent with recombination eroding nuclear donor ancestry while captured cytoplasmic genomes persist. Dioecy was associated with genome-wide shifts in selection intensity, with positive selection concentrated on the stems of each dioecious clade but targeting largely non-overlapping genes and leaving little signature within sex-determining regions. Plastid coding sequences evolved under relaxed purifying selection, and nuclear-encoded plastid-targeted genes were enriched for episodic positive selection, consistent with compensatory cytonuclear evolution. The probable reversion to monoecy in A. pumilus, within a lineage shaped by repeated organelle capture, raises the possibility that hybridization and the lability of separate sexes are connected in this group.

evolutionary biology↗

From recognition to neglect: Molecular and physiological responses to heterospecific pollen decay with evolutionary distance

Post-mating, pre-zygotic (PMPZ) reproductive barriers are often attributed to precise molecular recognition between male and female gametes, yet little is known about how these interactions change as species diverge. In flowering plants, pollen tube growth depends on coordinated signaling between pollen and pistil, raising the question of whether PMPZ barriers arise through active incompatibility mechanisms or gradual loss of pollen-pistil coordination. Here, we combined transcriptomic profiling and pollen tube growth assays across a phylogenetically structured set of crosses in a diverse alpine plant community. We show that the magnitude of the pistillar transcriptomic response to pollination declined quantitatively with evolutionary distance rather than shifting in a binary compatible/incompatible manner. Pollination-associated functional gene ontology categories were strongest in conspecific and intrageneric crosses and weakened with divergence. Heterospecific pollen tubes also grew more slowly than conspecific tubes, with growth rates declining overall with genetic distance. However, the slowest growth occurred in intrageneric crosses, suggesting that close relatives may represent a distinct evolutionary zone where reduced maternal support coincides with additional hindrance mechanisms. Together, these results support a graded, divergence-dependent model of pollen-pistil incongruence driven primarily by attenuation of coordinated growth rather than strict heterospecific rejection.

evolutionary biology↗

A reference genome and transcriptome of haustorial development in Pedicularis groenlandica reveal diverse trajectories of haustoria-associated gene evolution in parasitic plants

O_LINovel traits frequently evolve by co-opting existing genetic pathways through direct repurposing of existing genes or neofunctionalization of duplicated genes. Parasitism represents a major innovation in plants, where a novel organ--the haustorium--evolved to penetrate hosts and extract water and nutrients. Previous studies hypothesized that haustoria-associated genes primarily evolve from root and pollen-associated pathways. C_LIO_LITo examine evolutionary trajectories of haustoria-associated genes, we generated a chromosome-scale genome of Pedicularis groenlandica (Orobanchaceae) and sampled transcriptomes throughout haustorial development. We examined differential expression of haustoria-associated genes and their paralogs and investigated orthology among haustoria-associated genes in five parasitic plants. C_LIO_LIWe identified 5,635 haustoria-associated genes in P. groenlandica, of which a greater proportion were associated with pollen tubes (67%) than roots (33%), evidenced by being differentially expressed in pollen tubes, nested within pollen tube-associated gene families, or both. Haustoria-associated genes with paralogs that arose after the evolution of parasitism in Orobanchaceae are more likely to be uniquely expressed in haustoria, consistent with neofunctionalization. C_LIO_LIOur results support both pleiotropy and neofunctionalization as mechanisms by which genetic pathways are co-opted for haustorial function. Haustoria-associated genes are highly lineage-specific, highlighting a dynamic and ongoing process of haustorial co-option of genes among parasitic plant lineages. C_LI

evolutionary biology↗

Estimating Waiting Distances Between Genealogy Changes under a Multi-Species Extension of the Sequentially Markov Coalescent

Genomes are composed of a mosaic of segments inherited from different ancestors, each separated by past recombination events. Consequently, genealogical relationships among multiple genomes vary spatially across different genomic regions. Expectations for the amount of genealogical variation among unlinked (uncorrelated) genomic regions is well described for either a single population (coalescent) or multiple structured populations (multispecies coalescent). However, the expected similarity among genealogies at linked regions of a genome is less well characterized. Recently, an analytical solution was derived for the expected distribution of waiting distances between changes in genealogical trees spatially across a genome for a single population with constant effective population size. Here we describe a generalization of this result, in terms of the expected distribution of waiting distances between changes in genealogical trees and topologies, for multiple structured populations with branch-specific effective population sizes (i.e., under the multispecies coalescent). Our solutions establish an expectation for genetic linkage in multispecies datasets and provide a new likelihood framework for linking demographic models with local ancestry inference across genomes.

evolutionary biology↗

Pollinator and host sharing lead to hybridization and introgression in Panamanian free-standing figs, but not in their pollinator wasps

Obligate pollination mutualisms, in which plant and pollinator lineages depend on each other for reproduction, often exhibit high levels of species-specificity. However, cases in which two or more pollinator species share a single host species (host sharing), or two or more host species share a single pollinator species (pollinator sharing), are known to occur in current ecological time. Further, evidence for host switching in evolutionary time is increasingly being recognized in these systems. The degree to which departures from strict specificity differentially affect the potential for hybridization and introgression in the associated host or pollinator is unclear. We addressed this question using genome-wide sequence data from five sympatric Panamanian free-standing fig species (Ficus subgenus Pharmacosycea, section Pharmacosycea) and their six associated fig pollinator wasp species (Tetrapus). Two of the five fig species, F. glabrata and F. maxima, were found to regularly share pollinators. In these species, ongoing hybridization was demonstrated by the detection of several first-generation (F1) hybrid individuals and historical introgression was indicated by phylogenetic network analysis. In contrast, although two of the pollinator species regularly share hosts, all six species were genetically distinct and deeply divergent, with no evidence for either hybridization or introgression. This pattern is consistent with results from other obligate pollination mutualisms, suggesting that, in contrast to their host plants, pollinators appear to be reproductively isolated, even when different species of pollinators mate in shared hosts.

evolutionary biology↗

Comparative genomics in Orobanchaceae provides insight into the origin and evolution of plant parasitism

Orobanchaceae is the largest family of parasitic plants, containing autotrophic and parasitic plants with all degrees of parasitism. This makes it by far the best family for studying the origin and evolution of plant parasitism. Here we provide three high-quality genomes of orobanchaceous plants, the autotrophic Lindenbergia luchunensis and the holoparasitic plants Phelipanche aegyptiaca and Orobanche cumana. Phylogenomic analysis of these three genomes together with those previously published and the transcriptomes of other orobanchaceous species, created a robust phylogenetic framework for Orobanchaceae. We found that an ancient whole-genome duplication (WGD; about 73.48 Mya), which occurred earlier than the origin of Orobanchaceae, might have contributed to the emergence of parasitism. However, no WGD events occurred in any lineage of orobanchaceous parasites except for Striga after divergence from their autotrophic common ancestor, suggesting that, in contrast to previous speculations, WGD is not associated with the emergence of holoparasitism. We detected evident convergent gene loss in all parasites within Orobanchaceae and between Orobanchaceae and dodder Cuscuta australis. The gene families in the orobanchaceous parasites showed a clear pattern of recent gains and expansions. The expanded gene families are enriched in functions related to the development of the haustorium, suggesting that recent gene family expansions may have facilitated the adaptation of orobanchaceous parasites to different hosts. This study illustrates a stepwise pattern in the evolution of parasitism in the orobanchaceous parasites, and will facilitate future studies on parasitism and the control of parasitic plants in agriculture.

plant biology↗

Genetic incompatibilities do not snowball in a demographic model of speciation

Two populations evolving in isolation can accumulate genetic differences over time that cause incompatibilities in their hybrid offspring. These "Dobzhansky-Muller incompatibilities" (DMIs) are predicted to accumulate at a rate faster than linear as the number of incompatible gene interactions "snowballs". Here we show that this snowball prediction is an artifact of two unrealistic modeling assumptions that stem from ignoring demography. We introduce a new alternative "demographic speciation model" in which the rate of DMI accumulation between populations is affected by the efficiency of purifying selection to remove incompatibilities that arise within populations. This model yields new testable predictions for understanding the tempo and mode of speciation based on population demographic parameters. A large-scale empirical analysis of bird and mammal datasets supports a unique prediction of our model: a negative relationship between effective population sizes and speciation rates. Our results challenge views of the snowball theory, and of ecological speciation models rooted in positive selection, showing instead that purifying selection may play a major role in mediating speciation rates.

evolutionary biology↗

The Multispecies Coalescent in Space and Time

A key distinction between species tree inference under the multi-species coalescent model (MSC), and the inference of gene trees in sliding windows along a genome, is in the effect of genetic linkage. Whereas the MSC explicitly assumes genealogies to be unlinked, i.e., statistically independent, genealogies located close together on genomes are spatially auto-correlated. Here we use tree sequence simulations with recombination to explore the effects of species tree parameters on spatial patterns of linkage among genealogies. We decompose coalescent time units to demonstrate differential effects of generation time and effective population size on spatial coalescent patterns, and we define a new metric, "phylogenetic linkage," for measuring the rate of decay of phylogenetic similarity by comparison to distances among unlinked genealogies. Finally, we provide a simple example where accounting for phylogenetic linkage in sliding window analyses improves local gene tree inference.

evolutionary biology↗

ipcoal: An interactive Python package for simulating and analyzing genealogies and sequences on a species tree or network

Summaryipcoal is a free and open source Python package for simulating and analyzing genealogies and sequences. It automates the task of describing complex demographic models (e.g., with divergence times, effective population sizes, migration events) to the msprime coalescent simulator by parsing a user-supplied species tree or network. Genealogies, sequences, and metadata are returned in tabular format allowing for easy downstream analyses. ipcoal includes phylogenetic inference tools to automate gene tree inference from simulated sequence data, and visualization tools for analyzing results and verifying model accuracy. The ipcoal package is a powerful tool for posterior predictive data analysis, for methods validation, and for teaching coalescent methods in an interactive and visual environment. Availability and implementationSource code is available from the GitHub repository (https://github.com/pmckenz1/ipcoal/) and is distributed for packaged installation with conda. Complete documentation and interactive notebooks prepared for teaching purposes are available at https://ipcoal.readthedocs.io/.

bioinformatics↗

Joint phylogenetic estimation of geographic movements and biome shifts during the global diversification of Viburnum

Phylogeny, fossils, biogeography, and biome occupancy provide evidence that reflects the singular evolutionary history of a clade. Despite the connections that bind them together, these lines of evidence are most often studied separately, by first inferring a fossil-dated molecular phylogeny, then mapping on ancestral ranges and biomes inferred from extant species. Here we jointly model the evolution of biogeographic ranges, biome affinities, and molecular sequences, incorporating fossils to estimate a dated phylogeny for all of the 163 extant species of the woody plant clade Viburnum (Adoxaceae) that we currently recognize. Our analyses indicate that while the major Viburnum lineages evolved in the Eocene, the majority of extant species originated since the Miocene. Viburnum radiated first in Asia, in warm, broad-leaved evergreen (lucidophyllous) forests. Within Asia we infer several early shifts into more tropical forests, and multiple shifts into forests that experience prolonged freezing. From Asia we infer two early movements into the New World. These two lineages probably first occupied warm temperate forests and adapted later to spreading cold climates. One of these lineages (Porphyrotinus) occupied cloud forests and moved south through the mountains of the Neotropics. Several other movements into North America took place more recently, facilitated by prior adaptations to freezing in the Old World. We also infer four disjunctions between Asia and Europe: the Tinus lineage is the oldest and probably occupied warm forests when it spread, while the other three were more recent and in cold-adapted lineages. These results variously contradict published accounts, especially the view that Viburnum radiated initially in cold forests and, accordingly, maintained vessel elements with scalariform perforations. We explored how the location and biome assignments of fossils affected our inference of ancestral areas and biome states. Our results are sensitive to, but not entirely dependent upon, the inclusion of fossil biome data. We argue that it will be critical to take advantage of all available lines of evidence to decipher events in the distant past, and the joint estimation approach developed here provides cautious hope even when fossil evidence is limited.

evolutionary biology↗

Inferring Processes of Coevolutionary Diversification in a Community of Panamanian Strangler Figs and Associated Pollinating Wasps

1The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically important, and ancient (~80-90 Ma), providing model systems for generating and testing many questions in evolution and ecology. Once thought to be a prime example of strict one-to-one cospeciation, current thinking suggests that genera of pollinator wasps co-evolve with corresponding subsections of figs, but the degree to which cospeciation or other processes contributes to the association at finer scales is unclear. Here we use genome-wide sequence data from a community of Panamanian strangler figs (Ficus subgenus Urostigma, section Americana) and associated fig wasp pollinators (Pegoscapus spp.) to infer the process of coevolutionary diversification in this obligate mutualism. Using a model-based approach adapted from the study of gene family evolution, our results indicate pervasive and ongoing host switching of pollinator wasps at this fine phylogenetic and regional scale. Although the model estimates a modest amount of cospeciation, simulations reveal this signal to be consistent with levels of co-association expected under a model of free host switching. Our findings provide an outline for testing how ecological and evolutionary processes can be modeled to evaluate the history of association of interacting lineages in a phylogenetic framework.

evolutionary biology↗