Heredity

Grigoriadou Zormpa, Ourania; Wilhelmi, Selina; Vucetic, Boban; Ciocîrlan, Mihnea-Ioan-Cezar; Mueller, Markus; Ciocîrlan, Elena; Curtu, Alexandru Lucian; Targem, Mehdi Ben; Wildhagen, Henning; Gailing, Oliver; Budde, Katharina B.

doi: 10.1038/s41437-025-00776-8pmid: 40571728

Differences in environmental conditions can shape the level and distribution of intraspecific genetic variation between and within populations. Elevational gradients are characterised by strong variation in environmental conditions on a short spatial scale and provide an ideal setting to study the spatial distribution of genetic diversity. Therefore, we investigated the genetic diversity, fine-scale spatial genetic structure (FSGS) and spring phenology (bud burst) as a proxy for flowering of five European beech (Fagus sylvatica L.) populations along an elevational gradient, ranging from about 550 m to 1450 m a.s.l. in the Romanian Carpathians. Using microsatellite and genome-wide single nucleotide polymorphism (SNP) markers, we observed a slight decrease in genetic diversity with increasing elevation and low population differentiation. Furthermore, levels of FSGS decreased with elevation along the gradient. We could not detect any significant effects of spring phenological traits on the level of FSGS probably because many different environmental factors and processes vary over the years and contribute to shaping the FSGS. The slightly lower genetic diversity in high elevation populations may indicate stronger drift effects and could be due to the marginal ecological conditions and the lower abundance of beech. However, in these stands with less competing crowns and a more open forest structure, pollen dispersal might be longer ranging in this wind pollinated species which could contribute to a weaker FSGS. The knowledge about the level and structure of genetic variation along environmental gradients is crucial to inform forest and conservation management especially in the face of climate change.

Ravikanthachari, Nitin; Boggs, Carol L.

doi: 10.1038/s41437-025-00777-7pmid: 40610591

Specialist phytophagous insects have a narrow hostplant range for optimal development and survival. Mismatches between female oviposition preference and larval performance can lead to high fitness costs. Understanding the mechanistic basis of this decoupling can help us understand evolutionary constraints and aid in predicting outcomes of error-prone oviposition. We investigated the causes for preference-performance mismatches in a specialist native herbivore laying eggs on an invasive toxic plant. Transcriptomic analyses revealed host-plant-specific gene expression signatures in larvae feeding on different plants, while there was no differential gene expression in gustatory/olfactory organs of adult females with different oviposition preferences. However, genomic analysis revealed significant genetic differentiation in several genes underlying signal transduction in adult females with different oviposition preferences. The larvae feeding on toxic plants showed lower expression of specialized detoxification enzymes and higher expression of general digestive enzymes, indicating the inability of larvae to detoxify toxic compounds present in the toxic plants. We additionally found that genes related to successful detoxification and adaptive feeding were enriched in larvae feeding on native plants, while genes related to toxic responses, apoptosis, and accelerated development were enriched in larvae feeding on toxic plants. Our findings dissect the underlying mechanisms behind a preference-performance mismatch, quantifying the impact of error-prone oviposition on larval performance in a specialized species interaction.

McNeill, Jessica; Brandt, Nathan; Schwarzkopf, Enrique J.; Jimenez, Mili; Smukowski Heil, Caiti

doi: 10.1038/s41437-025-00778-6pmid: 40715475

Meiosis is required for the formation of gametes in all sexually reproducing species and the process is well conserved across the tree of life. However, meiosis is sensitive to a variety of external factors, which can impact chromosome pairing, recombination, and fertility. For example, the optimal temperature for successful meiosis varies between species of plants and animals. This suggests that meiosis is temperature sensitive, and that natural selection may act on variation in meiotic success as organisms adapt to different environmental conditions. To understand how temperature alters the successful completion of meiosis, we utilized two species of the budding yeast Saccharomyces with different temperature preferences: thermotolerant Saccharomyces cerevisiae and cold-tolerant Saccharomyces uvarum. We surveyed three metrics of meiosis: sporulation efficiency, spore viability, and recombination rate in multiple strains of each species. As per our predictions, the proportion of cells that complete meiosis and form spores is temperature sensitive, with thermotolerant S. cerevisiae having a higher temperature threshold for completion of meiosis than cold-tolerant S. uvarum. We confirmed previous observations that S. cerevisiae recombination rate varies between strains and across genomic regions, and add new results that S. uvarum has comparably high recombination rates. We find significant recombination rate plasticity due to temperature in S. cerevisiae and S. uvarum, in agreement with studies in animals and plants. Overall, these results suggest that meiotic thermal sensitivity is associated with organismal thermal tolerance and may even result in temporal reproductive isolation as populations diverge in thermal profiles.

Ahn, Ezekiel; Prom, Louis K.; Park, Sunchung; Lee, Dongho; Bhatt, Jishnu; Ellur, Vishnutej; Lim, Seunghyun; Jang, Jae Hee; Lakshman, Dilip; Magill, Clint

doi: 10.1038/s41437-025-00783-9pmid: 40684039

Plant disease resistance is often a complex, polygenic trait, making its genetic dissection with traditional genome-wide association studies (GWAS) challenging. Grain mold in sorghum, a devastating disease caused by a fungal complex, exemplifies this complexity. We hypothesized that a machine learning (ML)-driven GWAS, employing diverse phenotypic representations from a panel of 306 sorghum accessions, could more effectively unravel the genetic basis of resistance. Phenotypic data, including raw disease scores, a ‘difference phenotype’ (inoculated vs. control), and principal components, were analyzed using Boosted Tree and Bootstrap Forest models, demonstrating strong explanatory power for phenotypic variance when trained on the entire dataset. This ML-GWAS approach confirmed a highly polygenic architecture for grain mold resistance, identifying numerous SNPs across the sorghum genome. Notably, several SNPs were consistently associated with resistance across multiple analytical models and phenotypic representations. These robustly identified SNPs were frequently located near genes with predicted functions integral to plant defense. Gene ontology (GO) analyses of the candidate gene set confirmed enrichment in categories supporting roles in pathogen recognition, DNA repair, and stress response modulation, indicating a multifaceted defense mechanism. This study provides valuable candidate genes for breeding sorghum with enhanced grain mold resistance and offers a refined methodological framework for dissecting complex traits in this crop. The successful application of this ML-based strategy in sorghum suggests its potential utility for studying similar complex traits in other plant species.

Carimán, Paulina; Guillemin, Marie-Laure; Giles, Emily C.; Narváez, Gabriela; Suescún, Ana V.; Sáenz-Agudelo, Pablo

doi: 10.1038/s41437-025-00782-wpmid: 40739430

Decades of research in population genetics have revealed that genetic divergence between populations and species is not uniformly distributed throughout the genome but rather exhibits a high degree of heterogeneity. Two main conceptual models—allopatric divergence and divergence with gene flow—have been proposed to explain this variability under natural selection. Here, we investigate patterns of genomic divergence in three marine limpet species, Scurria scurra, Scurria araucana, and Scurria ceciliana, across two major biogeographic breaks (30–34°S and 41–43°S). Genomic divergence varied among species, even between the two sympatric species S. scurra and S. araucana, which exhibited heterogeneous divergence patterns across the 30–34°S range. In S. ceciliana, the southernmost species (41–43°S), divergence was shaped by a combination of allopatric divergence and divergence with gene flow. This was unexpected given that its evolutionary history suggests past isolation in glacial refugia, which would have limited gene flow. However, the observed genomic divergence indicates that genetic exchange occurred between populations, challenging previous assumptions about its evolutionary dynamics. Divergence patterns appear species-specific, with few shared genomic regions, though more similarities were found among the sister species S. scurra and S. araucana. In highly divergent regions, genes associated with lipid metabolism were identified in S. scurra and S. araucana, whereas genes related to oxidative stress response and mitochondrial functions were found in S. ceciliana. These findings suggest that genomic divergence is not entirely stochastic but may be shaped by different selective pressures in each species, potentially reflecting adaptation to distinct ecological conditions.

Numajiri, Yuko; Kondo, Natsuko I.; Toquenaga, Yukihiko; Kageyama, Daisuke

doi: 10.1038/s41437-025-00787-5pmid: 40739429

Cytoplasmic incompatibility (CI) is a phenomenon where embryonic development is disrupted–often leading to complete failure–when the female parent lacks the symbiont strain carried by the male parent. This mechanism, employed by maternally transmitted symbionts such as Wolbachia, facilitates their rapid spread within a host population. CI has significant potential as a tool for achieving population replacement or suppression, particularly targeting disease vectors and agricultural pests. While complete expression of CI is ideal for such applications, its intensity can vary. Despite extensive research on the symbiont genotypes, the influence of host genetic background on CI expression remains poorly understood. Here, we found that in the bean beetle Callosobruchus analis, the Wolbachia strain wCana2 induces weak CI in its native nuclear background but strong CI in a previously unassociated nuclear background. Crossing experiments reveal that the nuclear backgrounds of both male and female parents can significantly affect CI expression independent of Wolbachia titres in C. analis. These findings uncover novel perspectives on the host-symbiont interactions underlying CI and highlight the complexities to be addressed for its practical application.