Biology subjects

Groh, J. S.

Publications and source records attributed to Groh, J. S..

6 recordsLinked to original sources

bioRxiv2025

Balanced polymorphism in a floral transcription factor underlies an ancient rhythm of daily sex alternation in avocado

In avocado and certain wild relatives in Lauraceae, pollination occurs via a synchronized rhythm of floral sex timing between two hermaphroditic flowering types. A-type plants present female-phase flowers in the morning and male-phase flowers in the afternoon, while B-types show the complementary pattern, a form of heterodichogamy. We map this dimorphism in avocado to a genomic region overlapping a single strong candidate gene, SDMYB, where a dominant haplotype confers A-type flowering. SDMYB belongs to a subgroup of R2R3 MYB transcription factors established as key regulators of floral maturation in diverse species with links to circadian jasmonate signaling. Haplotypes at this locus form an ancient trans-species polymorphism maintained by negative frequency-dependent balancing selection over 44 million years, and they segregate in at least 26 non-avocado species, including in a genus where this mating system has not been reported. Across several species examined, rhythmic diel SDMYB expression is associated with biphasic floral anthesis, and the dominant allele, which contains nonsynonymous changes in conserved functional domains, exhibits a cis-regulated phase delay, corresponding to the delayed 2nd anthesis of A-types. The coupling of dichogamy with diel flower movements, widespread among magnoliids, is a likely precursor to daily forms of heterodichogamy. Absence of the SDMYB polymorphism in true cinnamon, which exhibits a highly similar mating system, suggests the possibility that heterodichogamy has convergently evolved within Lauraceae.

evolutionary biology↗

bioRxiv2025

Allelic turnover and dominance reversal at a single-gene balanced polymorphism controlling heterodichogamous flowering in wingnuts (Juglandaceae)

Angiosperms have evolved a wide variety of spatial and temporal developmental mechanisms to limit sexual interference and inbreeding. In heterodichogamy, two hermaphroditic morphs exploit distinct temporal reproductive niches by alternating phases of male and female flowering, promoting disassortative mating. This system is widespread within Juglandaceae, and known to be controlled by ancient balanced polymorphisms in walnuts (Juglans) and hickories (Carya). Here we identify distinct inheritance mechanisms controlling heterodichogamy in two separate Juglandaceae genera, the wingnuts (Pterocarya and Cyclocarya). We first document the occurrence of heterodichogamy in Pterocarya and map its genomic basis to haplotypes overlapping a single candidate gene in the FANTASTIC FOUR superfamily (GFAFL). These haplotypes segregate throughout the entire genus and the dominant haplotype controls female-first flowering. We show heterodichogamy in the sister genus Cyclocarya is associated with a distinct pair of ancient haplotypes at the same locus in both diploids and tetraploids, but with a dominant allele controlling male-first flowering. We infer a well-resolved fossil-calibrated phylogeny of Juglandaceae and date the divergence of the Pterocarya and Cyclocarya haplotypes to 51 and 44 million years ago, more recent than the divergence of these genera. In Pterocarya female-first heterozygotes, the dominant haplotype is associated with allele-specific suppression of the recessive copy of GFAFL during early male flower development. In Cyclocarya male-first heterozygotes, the dominant haplotype is associated with allele-specific activation of the recessive copy of GFAFL during male flower development, while the dominant copy itself shows higher expression in female flowers. We propose a model for the evolution of reciprocal sex matching in heterodichogamy through the combination of cis-regulatory divergence and allelic interactions involving fast and slow alleles at a single gene regulating flowering time. The non-independent expression of alleles in both systems is reminiscent of trans-sensing phenomena in other systems and suggests a mechanism mediated by DNA homology or an RNA intermediary. Notably, the dominant haplotypes in both genera show parallel architecture with a hemizygous region containing tandem duplicates of the same 1 kb motif downstream of the transcribed region of GFAFL which may be linked with such a mechanism. Our findings shed light on the molecular basis of heterodichogamy and contribute to an emerging view that diverse genetic pathways can be co-opted during its evolution and facilitate turnover in its genetic control.

evolutionary biology↗

bioRxiv2023

Genome evolution is surprisingly predictable after initial hybridization

Over the past two decades, evolutionary biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common - not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past [~]40 generations of evolution. Finally, we compare our results to the well-studied X. birchmannixX. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi.

evolutionary biology↗

bioRxiv2023

Distinct ancient structural polymorphisms control heterodichogamy in walnuts and hickories

The maintenance of stable mating type polymorphisms is a classic example of balancing selection, underlying the nearly ubiquitous 50/50 sex ratio in species with separate sexes. One lesser known but intriguing example of a balanced mating polymorphism in angiosperms is heterodichogamy - polymorphism for opposing directions of dichogamy (temporal separation of male and female function in hermaphrodites) within a flowering season. This mating system is common throughout Juglandaceae, the family that includes globally important and iconic nut and timber crops - walnuts (Juglans), as well as pecan and other hickories (Carya). In both genera, heterodichogamy is controlled by a single dominant allele. We fine-map the locus in each genus, and find two ancient (>50 Mya) structural variants involving different genes that both segregate as genus-wide trans-species polymorphisms. The Juglans locus maps to a ca. 20 kb structural variant adjacent to a probable trehalose phosphate phosphatase (TPPD-1), homologs of which regulate floral development in model systems. TPPD-1 is differentially expressed between morphs in developing male flowers, with increased allele-specific expression of the dominant haplotype copy. Across species, the dominant haplotype contains a tandem array of duplicated sequence motifs, part of which is an inverted copy of the TPPD-1 3 UTR. These repeats generate various distinct small RNAs matching sequences within the 3 UTR and further downstream. In contrast to the single-gene Juglans locus, the Carya heterodichogamy locus maps to a ca. 200-450 kb cluster of tightly linked polymorphisms across 20 genes, some of which have known roles in flowering and are differentially expressed between morphs in developing flowers. The dominant haplotype in pecan, which is nearly always heterozygous and appears to rarely recombine, shows markedly reduced genetic diversity and is over twice as long as its recessive counterpart due to accumulation of various types of transposable elements. We did not detect either genetic system in other heterodichogamous genera within Juglandaceae, suggesting that additional genetic systems for heterodichogamy may yet remain undiscovered.

evolutionary biology↗

bioRxiv2023

The temporal and genomic scale of selection following hybridization

1Genomic evidence supports an important role for selection in shaping patterns of introgression along the genome, but frameworks for understanding the dynamics underlying these patterns within hybrid populations have been lacking. Here, we develop methods based on the Wavelet Transform to understand the spatial genomic scale of local ancestry variation and its association with recombination rates. We present theory and use simulations to show how wavelet-based decompositions of ancestry variance along the genome and the correlation between ancestry and recombination reflect the joint effects of recombination, genetic drift, and genome-wide selection against introgressed alleles. Due to the clock-like effect of recombination in hybrids breaking up parental haplotypes, drift and selection produce predictable patterns of local ancestry variation at varying spatial genomic scales through time. Using wavelet approaches to identify the genomic scale of variance in ancestry and its correlates, we show that these methods can detect temporally localized effects of drift and selection. We apply these methods to previously published datasets from hybrid populations of swordtail fish (Xiphophorus) and baboons (Papio), and to inferred Neanderthal introgression in modern humans. Across systems, we find that upwards of 20% of the variation in local ancestry at the broadest genomic scales can be attributed to systematic selection against introgressed alleles, consistent with strong selection acting on early-generation hybrids. We also see signals of selection at fine genomic scales and much longer time scales. However, we show that our ability to confidently infer selection at fine scales is likely limited by inherent biases in current methods for estimating local ancestry from genomic similarity. Wavelet approaches will become widely applicable as genomic data from systems with introgression become increasingly available, and can help shed light on generalities of the genomic consequences of interspecific hybridization.

evolutionary biology↗

bioRxiv2020

Highly replicated evolution of parapatric ecotypes

Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origin of ecotypes is often inferred on the basis of a phylogeny which clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic because gene flow and incomplete lineage sorting can uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography and show that this is unlikely due to gene flow between parapatric ecotypes, which is surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.

evolutionary biology↗