Biology subjects

Finseth, F. R.

Publications and source records attributed to Finseth, F. R..

5 recordsLinked to original sources

bioRxiv2026

A centromere but not just a centromere: structure and evolution of a selfish chromosomal supergene in monkeyflowers

Meiotic drivers capitalize on vulnerabilities in eukaryotic meiosis and gametogenesis to gain greater-than-equal transmission to the next generation. In most plants and animals, asymmetric female meiosis is such an arena for selfishness; centromeric variants can bias their chromosomes segregation to the one egg cell with potentially profound effects on individual fitness, population dynamics, and genome structure. However, the mechanisms and consequences of selfish centromere evolution remain obscure, due to both the complexity of centromeric DNA and to a paucity of model systems. Here, we build on representative chromosome-scale assemblies of yellow monkeyflowers (M. guttatus species complex) to compare the structure, gene content, and sequence of three functionally distinct haplotypes at Meiotic Drive Locus on Chromosome 11 (MDL11), whose driving D allele was previously shown to be centromere-containing, costly, and maintained as a balanced polymorphism in wild populations. Relative to both moderately-resistant M. guttatus nondrivers (D-; IM767) and weak (d) M. nasutus, D minimally evolved via two rearrangements (including a hemicentric inversion creating dual arrays of M. guttatus centromeric satellite Cent728 separated by > 200 trapped genes), massive expansions of a novel MDL11-specific subfamily of satellite repeats (Cent728D) that increase D chromosome length by >50%, and the accumulation of >40 extra D-only genes (EDG) from diverse genomic sources in a hemizygous pericentromeric region. Under a strictly centromeric model of selfishness, the recent expansion of Cent728D is a primary candidate for generating centromere drive, either by directly altering the binding of centromeric histone CenH3 or by shifting kinetochore size or position as an epigenetic byproduct of chromosome size. However, elevated divergence in genic presence-absence variants (both in the EDG and elsewhere) and gene sequence across MDL11 strata points to strong candidates for both collusion with the D centromere and for interspecific (D- vs. d) variation in resistance. Overall, our findings support the sequential buildup of this model centromeric driver over time, reveal intriguing parallels with adaptive and gamete-killing supergenes, and provide a strong platform for further dissection of the molecular genetic basis of its dramatic deviations from Mendelian rules.

genetics↗

bioRxiv2024

Undoing the 'nasty: dissecting touch-sensitive stigma movement (thigmonasty) and its loss in self-pollinating monkeyflowers

Rapid touch-sensitive stigma closure is a novel plant reproductive trait found in hundreds of Lamiales species. The origins, mechanisms, and functions of stigma closure remain poorly understood, but its repeated loss in self-fertilizing taxa and direct tests implicate adaptive roles in animal-mediated cross-pollination. Here, we document several additional losses of stigma closure in monkeyflowers (Mimulus), then use quantitative trait locus (QTL) mapping and gene expression analyses to provide a first glimpse into the genetic and molecular basis of stigma mechanosensing and movement. Variation in stigma closure in hybrids between selfer/non-closer Mimulus nasutus and outcrosser/fast-closer M. guttatus has a moderately complex genetic basis, with four QTLs together explaining [~]70% of parental divergence.Loss of stigma closure in M. nasutus appears genetically independent from other aspects of the floral selfing syndrome and from a parallel loss in M. parishii. Analyses of stylar gene expression in closer M. guttatus, M. nasutus, and a rare M. guttatus non-closer genotype identify functional candidates involved in mechanosensing, turgor regulation, and cell wall remodeling. Together, these analyses reveal a polygenic genetic architecture underlying gain and loss of a novel plant movement, illuminate selfer-outcrosser reproductive divergence, and initiate mechanistic investigations of an unusually visible manifestation of plant intelligence.

plant biology↗

bioRxiv2020

Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers

Under the selfish centromere model, costs associated with female meiotic drive by centromeres select on interacting kinetochore proteins to restore Mendelian inheritance. We directly test this model in yellow monkeyflowers (Mimulus guttatus), which are polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. Quantitative genetic analyses reveal that variation in the strength of drive primarily depends on the identity of the non-D centromere, but also identified an unlinked modifier coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). CenH3A has also experienced a recent (<1000 years) selective sweep in our focal population, consistent with ongoing interactions with D shaping its evolution. Together, our results demonstrate an active co-evolutionary arms race between the DNA and protein components of the meiotic machinery, with important consequences for individual fitness and molecular divergence.

evolutionary biology↗

bioRxiv2020

Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Pattersons D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation. Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.

evolutionary biology↗

bioRxiv2018

Evolution of the highly repetitive PEVK region of titin across mammals

The protein titin plays a key role in vertebrate muscle where it acts like a giant molecular spring. Despite its importance and conservation over vertebrate evolution, a lack of high quality annotations in non-model species makes comparative evolutionary studies of titin challenging. The PEVK region of titin--named for its high proportion of Pro-Glu-Val-Lys amino acids--is particularly difficult to annotate due to its abundance of alternatively spliced isoforms and short, highly repetitive exons. To understand PEVK evolution across mammals, we first developed a bioinformatics tool, PEVK_Finder, to annotate PEVK exons from genomic sequences of titin and then applied it to a diverse set of mammals. PEVK_Finder consistently outperforms standard annotation tools across a broad range of conditions and improves annotations of the PEVK region in non-model mammalian species. We find that the PEVK region can be divided into two subregions (PEVK-N, PEVK-C) with distinct patterns of evolutionary constraint and divergence. The bipartite nature of the PEVK region has implications for titin diversification. In the PEVK-N region, certain exons are conserved and may be essential, but natural selection also acts on particular codons. This region is also rich in glutamate and may contribute to actin binding. In the PEVK-C, exons are more homogenous and length variation of the PEVK region may provide the raw material for evolutionary adaptation in titin function. Taken together, we find that the very complexity that makes titin a challenge for annotation tools may also promote evolutionary adaptation.

genomics↗