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1. Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species

   https://doi.org/10.1111/mec.17261  

   Mantel, Samuel J.; Sweigart, Andrea L. (January 2024, Molecular Ecology)

   Abstract The 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 naturally hybridizing species are not well understood. Here, we explore these issues using genetic mapping in three independent populations of recombinant inbred lines between naturally hybridizing monkeyflowers,Mimulus guttatusandMimulus nasutus,from the sympatric Catherine Creek population. We discover that the threeM. guttatusfounders differ dramatically in admixture history, with nearly a quarter of one founder's genome introgressed fromM. nasutus. Comparative genetic mapping in the three RIL populations reveals three new putative inversions, each one segregating among theM. guttatusfounders, two due to admixture. We find strong, genome‐wide transmission ratio distortion in all RILs, but patterns are highly variable among the three populations. At least some of this distortion appears to be explained by epistatic selection favouring parental genotypes, but tests of inter‐chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky‐Muller incompatibilities. We also map several genetic loci for hybrid pollen viability, including two interacting pairs that coincide with peaks of distortion. Remarkably, even with this limited sample of threeM. guttatuslines, we discover abundant segregating variation for hybrid incompatibilities withM. nasutus,suggesting this population harbours diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities betweenMimulusspecies persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system. 

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2. Absence of heterosis for hypoxia tolerance in F1 hybrids of Tigriopus californicus

   https://doi.org/10.1093/jhered/esae061  

   Deconinck, Aimee; Madalone, Olivia F; Willett, Christopher S (October 2024, Journal of Heredity)

   Delmore, Kira (Ed.)

   Abstract Hybridization produces a range of outcomes from advantageous to disadvantageous, and a goal of genetic research is to understand the gene interactions that generate these outcomes. Interactions between cytoplasmic elements, such as mitochondria, and the nucleus may be particularly vulnerable to accruing disadvantageous combinations as a result of their different rates of evolution. Consequently, mitonuclear incompatibilities may play an important role in hybrid outcomes even if their negative impacts could be masked for some fitness measures by heterosis in first-generation (F1) hybrids. We used Tigriopus californicus, a model system for mitonuclear incompatibilities that is also known for exhibiting heterosis in the F1 generation and outbreeding depression in later generations, to test whether heterosis or outbreeding depression would occur when mitonuclear mismatch was paired with a stress that heavily impacts mitochondrial processes—specifically, hypoxia. We generated 284 parental and 436 F1 hybrids from four population crosses (720 total) and compared parental and F1 populations for hypoxia tolerance. We observed that, on average, F1 hybrids were less likely to survive a hypoxia stress test than parental populations, although we did not detect a statistically significant trend (P = 0.246 to 0.614). This suggests that hypoxia may be a particularly intense stressor for mitonuclear coordination and hybridization outcomes vary by trait. 

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3. Genetic incompatibilities in reciprocal hybrids between populations of Tigriopus californicus with low to moderate mitochondrial sequence divergence

   https://doi.org/10.1093/evolut/qpad122  

   Healy, Timothy M.; Burton, Ronald S.; Montooth, ed., Kristi; Connallon, ed., Tim (July 2023, Evolution)

   Abstract All mitochondrial-encoded proteins and RNAs function through interactions with nuclear-encoded proteins, which are critical for mitochondrial performance and eukaryotic fitness. Coevolution maintains inter-genomic (i.e., mitonuclear) compatibility within a taxon, but hybridization can disrupt coevolved interactions, resulting in hybrid breakdown. Thus, mitonuclear incompatibilities may be important mechanisms underlying reproductive isolation and, potentially, speciation. Here we utilize Pool-seq to assess the effects of mitochondrial genotype on nuclear allele frequencies in fast- and slow-developing reciprocal inter-population F2 hybrids between relatively low-divergence populations of the intertidal copepod Tigriopus californicus. We show that mitonuclear interactions lead to elevated frequencies of coevolved (i.e., maternal) nuclear alleles on two chromosomes in crosses between populations with 1.5% or 9.6% fixed differences in mitochondrial DNA nucleotide sequence. However, we also find evidence of excess mismatched (i.e., noncoevolved) alleles on three or four chromosomes per cross, respectively, and of allele frequency differences consistent with effects involving only nuclear loci (i.e., unaffected by mitochondrial genotype). Thus, our results for low-divergence crosses suggest an underlying role for mitonuclear interactions in variation in hybrid developmental rate, but despite substantial effects of mitonuclear coevolution on individual chromosomes, no clear bias favoring coevolved interactions overall. 

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4. Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities

   https://doi.org/10.1111/mec.15985  

   Pereira, Ricardo J.; Lima, Thiago G.; Pierce‐Ward, N. Tessa; Chao, Lin; Burton, Ronald S. (June 2021, Molecular Ecology)

   Abstract Reproductive isolation is often achieved when genes that are neutral or beneficial in their genomic background become functionally incompatible in a foreign genomic background, causing inviability, sterility or other forms of low fitness in hybrids. Recent studies suggest that mitonuclear interactions are among the initial incompatibilities to evolve at early stages of population divergence across taxa. Yet, the genomic architecture of mitonuclear incompatibilities has rarely been elucidated. We employ an experimental evolution approach starting with low‐fitness F₂interpopulation hybrids of the copepodTigriopus californicus, in which frequencies of compatible and incompatible nuclear alleles change in response to an alternative mitochondrial background. After about nine generations, we observe a generalized increase in population size and in survivorship, suggesting efficiency of selection against maladaptive phenotypes. Whole genome sequencing of evolved populations showed some consistent allele frequency changes across three replicates of each reciprocal cross, but markedly different patterns between mitochondrial backgrounds. In only a few regions (~6.5% of the genome), the same parental allele was overrepresented irrespective of the mitochondrial background. About 33% of the genome showed allele frequency changes consistent with divergent selection, with the location of these genomic regions strongly differing between mitochondrial backgrounds. In 87% and 89% of these genomic regions, the dominant nuclear allele matched the associated mitochondrial background, consistent with mitonuclear co‐adaptation. These results suggest that mitonuclear incompatibilities have a complex polygenic architecture that differs between populations, potentially generating genome‐wide barriers to gene flow between closely related taxa. 

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5. A polygenic explanation for Haldane’s rule in butterflies

   https://doi.org/10.1073/pnas.2300959120  

   Xiong, Tianzhu; Tarikere, Shreeharsha; Rosser, Neil; Li, Xueyan; Yago, Masaya; Mallet, James (October 2023, Proceedings of the National Academy of Sciences)

   Two robust rules have been discovered about animal hybrids: Heterogametic hybrids are more unfit (Haldane’s rule), and sex chromosomes are disproportionately involved in hybrid incompatibility (the large-X/Z effect). The exact mechanisms causing these rules in female heterogametic taxa such as butterflies are unknown but are suggested by theory to involve dominance on the sex chromosome. We investigate hybrid incompatibilities adhering to both rules inPapilioandHeliconiusbutterflies and show that dominance theory cannot explain our data. Instead, many defects coincide with unbalanced multilocus introgression between the Z chromosome and all autosomes. Our polygenic explanation predicts both rules because the imbalance is likely greater in heterogametic females, and the proportion of introgressed ancestry is more variable on the Z chromosome. We also show that mapping traits polygenic on a single chromosome in backcrosses can generate spurious large-effect QTLs. This mirage is caused by statistical linkage among polygenes that inflates estimated effect sizes. By controlling for statistical linkage, most incompatibility QTLs in our hybrid crosses are consistent with a polygenic basis. Since the two genera are very distantly related, polygenic hybrid incompatibilities are likely common in butterflies. 

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