Biology subjects

Sweigart, A. L.

Publications and source records attributed to Sweigart, A. L..

12 recordsLinked to original sources

bioRxiv2026

On the causes of correlated genomic ancestry across contrasting hybridization histories in a monkeyflower species pair.

Hybridization is a powerful force shaping the evolutionary trajectories of species, yet its outcomes are highly variable both across taxa and within a pair of species. In this study, we examine the processes shaping variation in the extent of hybrid ancestry, both among populations and across the genome. We use low-coverage sequencing data to infer local ancestry across the genome for 782 individuals from multiple populations across two geographic regions within the broadly overlapping range of Mimulus guttatus and Mimulus nasutus. We find that the extent of hybrid ancestry is variable across populations, supporting disparate historical patterns of hybridization. However, genomic patterns of hybrid ancestry are correlated across groups, indicating they are shaped by parallel processes. Correlations are highest in geographically proximal populations, including between sympatric and allopatric locations, providing evidence that introgression is not locally constrained but spreads via migration across the landscape. We find that features of the genome are predictive of hybrid ancestry and its correlations among populations. However, contrary to findings in some other species, these patterns are likely not driven by simple linked selection against hybrid ancestry. Genomic outliers for high hybrid ancestry are often shared among populations, suggesting a role for parallel positive selection on ancestry. However, known loci associated with reproductive isolation are poor predictors of ancestry variation across populations, indicating that selection acting in natural hybrid populations is highly polygenic and that the underlying genetic architecture varies across space. Overall, this study demonstrates how ecological, demographic, and genomic features all interact to shape the outcomes of hybridization.

evolutionary biology↗

bioRxiv2024

Fluctuating reproductive isolation and stable ancestry structure in a fine-scaled mosaic of hybridizing Mimulus monkeyflowers

Hybridization among taxa impacts a variety of evolutionary processes from adaptation to extinction. We seek to understand both patterns of hybridization across taxa and the evolutionary and ecological forces driving those patterns. To this end, we use whole-genome low-coverage sequencing of 459 wild-grown and 1565 offspring individuals to characterize the structure, stability, and mating dynamics of admixed populations of Mimulus guttatus and Mimulus nasutus across a decade of sampling. In three streams, admixed genomes are common and a M. nasutus organellar haplotype is fixed in M. guttatus, but new hybridization events are rare. Admixture is strongly unidirectional, but each stream has a unique distribution of ancestry proportions. In one stream, three distinct cohorts of admixed ancestry are spatially structured at [~]20-50m resolution and stable across years. Mating system provides almost complete isolation of M. nasutus from both M. guttatus and admixed cohorts, and is a partial barrier between admixed and M. guttatus cohorts. Isolation due to phenology is near-complete between M. guttatus and M. nasutus. Phenological isolation is a strong barrier in some years between admixed and M. guttatus cohorts, but a much weaker barrier in other years, providing a potential bridge for gene flow. These fluctuations are associated with differences in water availability across years, supporting a role for climate in mediating the strength of reproductive isolation. Together, mating system and phenology accurately predict fluctuations in assortative mating across years, which we estimate directly using paired maternal and offspring genotypes. Climate-driven fluctuations in reproductive isolation may promote the longer-term stability of a complex mosaic of hybrid ancestry, preventing either complete isolation or complete collapse of species barriers. Author SummaryHybridization between species can create genetic novelty and promote adaptation, but can also erode species barriers and dilute genetic diversity. Climatic variation likely impacts the extent and eventual outcomes of hybridization, but these impacts are difficult to predict. We use population-scale genomic sequencing of hybridizing Mimulus monkeyflowers to better understand the influence of climatic variation on hybridization. We find evidence of hybridization in multiple populations, with groups of different hybrid ancestries clustered along streams in close proximity to each other. Variation in water availability across years appears to affect hybridization between these groups, with less hybridization in drier years compared to wetter years. Paradoxically, this variation may lead to longer-term stability of the hybridization populations, by preventing complete erosion of species barriers while still allowing some gene exchange. In fact, we do see that hybrid ancestry is remarkably stable across a decade of measurements. Climate change is expected to increase the variability of climatic factors such as precipitation and heat events. Our study demonstrates one way these fluctuations could impact species.

evolutionary biology↗

bioRxiv2024

The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

O_LIPollination syndromes are a key component of flowering plant diversification, prompting questions about the architecture of single traits and genetic coordination among traits. Here, we investigate the genetics of extreme floral divergence between naturally hybridizing monkeyflowers Mimulus parishii (self-pollinated) and M. cardinalis (hummingbird-pollinated). C_LIO_LIWe mapped quantitative trait loci (QTLs) for 18 pigment, pollinator reward/handling, and dimensional traits in parallel sets of F2 hybrids plus recombinant inbred lines and generated nearly isogenic lines (NILs) for two dimensional traits, pistil length and corolla size. C_LIO_LIOur multi-population approach revealed a highly polygenic basis (n = 190 QTLs total) for pollination syndrome divergence, capturing minor QTLs even for pigment traits with leading major loci. There was significant QTL overlap within pigment and dimensional categories. Nectar volume QTLs clustered with those for floral dimensions, suggesting a partially shared module. The NILs refined two pistil length QTLs, only one of which has tightly correlated effects on other dimensional traits. C_LIO_LIAn overall polygenic architecture of floral divergence is partially coordinated by genetic modules formed by linkage (pigments) and likely pleiotropy (dimensions plus nectar). This work illuminates pollinator syndrome evolution in a model radiation and generates a robust framework for molecular and ecological genomics. C_LI

evolutionary biology↗

bioRxiv2023

Patterns of genomic variation reveal a single evolutionary origin of the wild allotetraploid Mimulus sookensis

Polyploidy occurs across the tree of life and is especially common in plants. Because newly formed cytotypes are often incompatible with their progenitors, polyploidy is also said to trigger "instantaneous" speciation. If a polyploid can self-fertilize or reproduce asexually, it is even possible for one individual to produce an entirely new lineage. How often this extreme scenario occurs is unclear, with most studies of wild polyploids reporting multiple origins. Here, we explore the evolutionary history of the wild allotetraploid Mimulus sookensis, which was formed through hybridization between self-compatible, diploid species in the Mimulus guttatus complex. We generate a chromosome-scale reference assembly for M. sookensis and define its distinct subgenomes. Despite previous reports suggesting multiple origins of this highly selfing polyploid, we discover patterns of population genomic variation that provide unambiguous support for a single origin, which we estimate occurred [~]71,000 years ago. One M. sookensis subgenome is clearly derived from the selfer M. nasutus, which, based on organellar variation, also appears to be the maternal progenitor. The ancestor of the other subgenome is less certain, but it shares variation with both M. decorus and M. guttatus, two outcrossing diploids that overlap broadly with M. sookensis. Whatever its precise ancestry, this study establishes M. sookensis as an example of instantaneous speciation, likely facilitated by the polyploids predisposition to self-fertilize. With a reference genome for M. sookensis now available and its origin clarified, this wild tetraploid is poised to become a model for understanding the genetic and evolutionary mechanisms of polyploid persistence.

evolutionary biology↗

bioRxiv2023

Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species

O_LIThe evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in sympatric species are not well understood. C_LIO_LIHere, we explore these issues using genetic mapping in three populations of recombinant inbred lines between naturally hybridizing monkeyflowers Mimulus guttatus and M. nasutus from the sympatric Catherine Creek population. C_LIO_LIThe three M. guttatus founders differ dramatically in admixture history. Comparative genetic mapping also reveals three putative inversions segregating among the M. guttatus founders, two due to admixture. We observe strong, genome-wide transmission ratio distortion, but patterns are highly variable among populations. Some distortion is explained by epistatic selection favoring parental genotypes, but tests of inter-chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky-Muller incompatibilities. We also map several genetic loci for hybrid fertility, including two interacting pairs coinciding with peaks of distortion. C_LIO_LIRemarkably, in this limited sample of M. guttatus, we discover abundant segregating variation for hybrid incompatibilities with M. nasutus, suggesting this population harbors diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities between Mimulus species persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system. C_LI

genetics↗

bioRxiv2022

Strong postmating reproductive isolation in Mimulus section Eunanus

Postmating reproductive isolation can help maintain species boundaries when premating barriers to reproduction are incomplete. The strength and identity of postmating reproductive barriers are highly variable among diverging species, leading to questions about their genetic basis and evolutionary drivers. These questions have been tackled in model systems but are less often addressed with broader phylogenetic resolution. In this study we analyze patterns of genetic divergence alongside direct measures of postmating reproductive barriers in an overlooked group of sympatric species within the model monkeyflower genus, Mimulus. Within this Mimulus brevipes species group, we find substantial divergence among species, including a cryptic genetic lineage. However, rampant gene discordance and ancient signals of introgression suggest a complex history of divergence. In addition, we find multiple strong postmating barriers, including postmating prezygotic isolation, hybrid seed inviability, and hybrid male sterility, leading to complete or substantial postmating isolation in all species pairs. Hybrid seed inviability appears linked to differences in seed size, providing a window into possible developmental mechanisms underlying this reproductive barrier. While geographic proximity and incomplete mating isolation may have allowed gene flow within this group in the distant past, strong postmating reproductive barriers today are likely to prevent any ongoing hybridization. By producing foundational information about reproductive isolation and genomic divergence in this understudied group, we add new diversity and phylogenetic resolution to our understanding of the mechanisms of plant speciation.

evolutionary biology↗

bioRxiv2022

Developmental evidence for parental conflict in driving Mimulus species barriers

The endosperm, a tissue that nourishes the embryo in the seeds of flowering plants, is often disrupted in inviable hybrid seeds between species presumed to have divergent histories of parental conflict. Despite the potential importance of parental conflict in plant speciation, we lack direct evidence of its action in driving species barriers. Here, we performed reciprocal crosses between pairs of three monkeyflower species (Mimulus caespitosa, M. tilingii, and M. guttatus). The severity of hybrid seed inviability varies among these crosses, which we determined was due to species divergence in effective ploidy. By performing a time series of seed development, we assessed whether regions within the endosperm were potential targets of parental conflict. We found that the chalazal haustorium, a tissue within the endosperm that occurs at the maternal-filial boundary, develops abnormally in hybrid seeds when the paternal parent has the greater effective ploidy. Within these Mimulus species, parental conflict might target the chalazal haustorium to control sucrose movement from the maternal parent into the endosperm. Consequently, conflict may be exposed in crosses between species. Our study suggests that parental conflict in the endosperm may function as a driver of speciation by targeting regions and developmental stages critical for resource allocation.

evolutionary biology↗

bioRxiv2020

Evolution of multiple postzygotic barriers between species in the Mimulus tilingii species complex

Species are often defined by their ability to interbreed (i.e., Biological Species Concept), but determining how and why reproductive isolation arises between new species can be challenging. In the Mimulus tilingii species complex, three species (M. caespitosa, M. minor, and M. tilingii) are largely allopatric and grow exclusively at high elevations (>2000m). The extent to which geographic separation has shaped patterns of divergence among the species is not well understood. In this study, we determined that the three species are morphologically and genetically distinct, yet recently diverged (<400kya). Additionally, we performed reciprocal crosses within and between the species and identified several strong postzygotic reproductive barriers, including hybrid seed inviability, F1 hybrid necrosis, and F1 hybrid male and female sterility. In this study, such postzygotic barriers are so strong that a cross between any species pair in the M. tilingii complex would cause nearly complete reproductive isolation. We consider how geographical and topographical patterns may have facilitated the evolution of several postzygotic barriers and contributed to speciation of closely related members within the M. tilingii species complex.

evolutionary biology↗

bioRxiv2019

Genome-wide misexpression associated with hybrid sterility in Mimulus (monkeyflower)

Divergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between Mimulus guttatus and M. nasutus, two closely related yellow monkeyflower species, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We quantified and compared global transcript abundance across male and female reproductive tissues (i.e. stamens and carpels) of M. guttatus and M. nasutus, as well as sterile and fertile progeny from an advanced M. nasutus-M. guttatus introgression line that carries the hms1-hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. Furthermore, we found pervasive genome-wide misexpression exclusively associated with hybrid sterility - only observed in the affected tissues (i.e. stamens) of sterile introgression hybrids. Examining patterns of allele-specific expression in sterile and fertile hybrids, we found evidence of cis- and trans- regulatory divergence, as well as cis-trans compensatory evolution (likely to be driven by stabilizing selection). However, regulatory divergence does not appear to cause misexpression in sterile hybrids, which instead likely manifests as a downstream consequence of sterility itself.

evolutionary biology↗

bioRxiv2018

A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus

Reproductive isolation, which is essential for the maintenance of species in sympatry, is often incomplete between closely related species. In these taxa, reproductive barriers must continue to evolve within species, without being degraded by ongoing gene flow. To better understand this dynamic, we investigated the frequency and distribution of incompatibility alleles at a two-locus, recessive-recessive hybrid lethality system between species of yellow monkeyflower (Mimulus guttatus and M. nasutus) that hybridize in nature. We found that M. guttatus typically carries hybrid lethality alleles at one locus (hl13) and M. nasutus typically carries hybrid lethality alleles at the other locus (hl14). As a result, most naturally formed hybrids will carry incompatible alleles at both loci, with the potential to express hybrid lethality in later generations. Despite this general pattern, we also discovered considerable polymorphism at both hl13 and hl14 within both Mimulus species. For M. guttatus, polymorphism at both loci even occurs within populations, meaning that incompatible allele pairings might also often arise through regular, intraspecific gene flow. By examining genetic variation linked to hl13 and hl14, we discovered that introgression from M. nasutus is a primary driver of this polymorphism within M. guttatus. Additionally, patterns of introgression at the two hybrid lethality loci suggest that natural selection acts to eliminate incompatible allele pairings, providing evidence that even weak reproductive barriers might promote genomic divergence between species.

evolutionary biology↗

bioRxiv2017

Gene duplicates cause hybrid lethality between sympatric species of Mimulus

Hybrid incompatibilities play a critical role in the evolution and maintenance of species. We have discovered a simple genetic incompatibility that causes lethality in hybrids between two closely related species of yellow monkeyflower (Mimulus guttatus and M. nasutus). This hybrid incompatibility, which causes one sixteenth of F2 hybrid seedlings to lack chlorophyll and die shortly after germination, occurs between sympatric populations that are connected by ongoing interspecific gene flow. Using complimentary genetic mapping and gene expression analyses, we show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene pTAC14. In M. guttatus, this gene was duplicated, but the ancestral copy is no longer expressed. In M. nasutus, the duplication is missing altogether. As a result, hybrids die when they are homozygous for the nonfunctional M. guttatus copy and missing the duplicate from M. nasutus, apparently due to misregulated transcription of key photosynthetic genes. Our study indicates that neutral evolutionary processes may play an important role in the evolution of hybrid incompatibilities and opens the door to direct investigations of their contribution to reproductive isolation among naturally hybridizing species.\n\nAuthor SummaryHybrid incompatibilities play an important role in speciation, because they act to limit gene flow between species. Identifying the genes that underlie these barriers sheds light on the evolutionary forces and genetic mechanisms that give rise to new species. We identified a reproductive barrier that causes lethality in the F2 offspring of sympatric species of yellow monkeyflower (Mimulus guttatus and M. nasutus). We show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene pTAC14. This gene was duplicated in M. guttatus, but the ancestral copy subsequently lost function. In M. nasutus, no duplication occurred. As a consequence, F2 hybrids that are homozygous for non-functional M. guttatus copies at one locus and missing M. nasutus duplicates at the other locus completely lack functional pTAC14 and die. Our data indicate that non-functionalization of ancestral pTAC14 in M. guttatus occurred via neutral evolutionary change. These results suggest that neutral evolutionary forces may play an important role in speciation.

evolutionary biology↗

bioRxiv2017

Mechanisms of transmission ratio distortion at hybrid sterility loci within and between Mimulus species

Hybrid incompatibilities are a common correlate of genomic divergence and a potentially important contributor to reproductive isolation. However, we do not yet have a detailed understanding of how hybrid incompatibility loci function and evolve within their native species, or why they are dysfunctional in hybrids. Here, we explore these issues for a well-studied, two-locus hybrid incompatibility between hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2) in the closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. By performing reciprocal backcrosses with introgression lines, we find evidence for gametic expression of the hms1-hms2 incompatibility. Surprisingly, however, hybrid transmission ratios at hms1 do not reflect this incompatibility, suggesting additional mechanisms counteract the effects of gametic sterility. Indeed, our backcross experiment shows hybrid transmission bias toward M. guttatus through both pollen and ovules, an effect that is particularly strong when hms2 is homozygous for M. nasutus alleles. In contrast, we find little evidence for hms1 transmission bias in crosses within M. guttatus, providing no indication of selfish evolution at this locus. Although we do not yet have sufficient genetic resolution to determine if hybrid sterility and transmission ratio distortion map to the same loci, our preliminary fine-mapping uncovers a genetically independent hybrid lethality system involving at least two loci linked to hms1. This fine-scale dissection of transmission ratio distortion at hms1 and hms2 provides insight into genomic differentiation between closely related Mimulus species and reveals multiple mechanisms of hybrid dysfunction.

evolutionary biology↗