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1. Genomic mechanisms and consequences of diverse postzygotic barriers between monkeyflower species

   https://doi.org/10.1093/genetics/iyad156  

   Sotola, V Alex; Berg, Colette S; Samuli, Matthew; Chen, Hongfei; Mantel, Samuel J; Beardsley, Paul A; Yuan, Yao-Wu; Sweigart, Andrea L; Fishman, Lila (August 2023, GENETICS)

   Moyle, L (Ed.)

   Abstract The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take 2 general forms—structural divergence between chromosomes leading to severe hybrid sterility in F1 hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky–Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2 and recombinant inbred line (RIL) hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowers Mimulus cardinalis and M. parishii to characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (<50% reduction vs parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and interchromosomal linkage disequilibrium in both F2s and RILs identified a novel 2-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction eliminated 3 of the expected 9 F2 genotypic classes via F1 gamete loss without detectable effects on the pollen number or viability of F2 double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system. 

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2. Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish Ictalurus punctatus and the Blue Catfish Ictalurus furcatus

   https://doi.org/10.3390/biology11010117  

   Wang, Haolong; Bruce, Timothy J.; Su, Baofeng; Li, Shangjia; Dunham, Rex A.; Wang, Xu (January 2022, Biology)

   The hybrid between female channel catfish (Ictalurus punctatus) and male blue catfish (Ictalurus furcatus) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobeltiosis only occur in pond culture, and channel catfish grow much faster than the other genetic types in small culture units. This environment-dependent heterosis is intriguing, but the underlying genetic mechanisms are not well understood. In this study, phenotypic characterization and transcriptomic analyses were performed in the channel catfish, blue catfish, and their reciprocal F1s reared in tanks. The results showed that the channel catfish is superior in growth-related morphometrics, presumably due to significantly lower innate immune function, as investigated by reduced lysozyme activity and alternative complement activity. RNA-seq analysis revealed that genes involved in fatty acid metabolism/transport are significantly upregulated in channel catfish compared to blue catfish and hybrids, which also contributes to the growth phenotype. Interestingly, hybrids have a 40–80% elevation in blood glucose than the parental species, which can be explained by a phenomenon called transgressive expression (overexpression/underexpression in F1s than the parental species). A total of 1140 transgressive genes were identified in F1 hybrids, indicating that 8.5% of the transcriptome displayed transgressive expression. Transgressive genes upregulated in F1s are enriched for glycan degradation function, directly related to the increase in blood glucose level. This study is the first to explore molecular mechanisms of environment-dependent heterosis/heterobeltiosis in a vertebrate species and sheds light on the regulation and evolution of heterosis vs. hybrid incompatibility. 

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3. Reduced hybrid survival in a migratory divide between songbirds

   https://doi.org/10.1111/ele.14420  

   Blain, Stephanie_A; Justen, Hannah_C; Easton, Wendy; Delmore, Kira_E (April 2024, Ecology Letters)

   Abstract Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile‐specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation. 

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4. Lower survival of hybrid grosbeaks, but not towhees, suggests a molt divide disfavors hybrids

   https://doi.org/10.1093/evolut/qpad112  

   Rohwer, Vanya G.; Hagler, Samantha J.; Van Doren, Benjamin M.; Fuentes, Miguel; Billerman, Shawn M.; Linnen, ed., Catherine; Zelditch, ed., Miriam (June 2023, Evolution)

   Abstract Although avian hybrid zones in the Great Plains have been studied for almost 70 years, we know surprisingly little about the fitness costs to hybrids that keep these zones narrow. We compare age ratios in grosbeaks (Pheucticus ludovicianus and P. melanocephalus) and towhees (Pipilo erythropthalums and P. maculatus), two species pairs that differ in their life histories and molt schedules, to evaluate survival between hybrids and parentals. We then contrast molt and migratory divides as possible sources of selection against hybrids. Hybrid grosbeaks had 27%–33% lower survival relative to their parentals, whereas hybrid towhees had survival rates similar to parentals. Age ratio data for hybrid grosbeaks suggest high mortality in older birds, as expected if selection operates after the first year of life. This pattern is consistent with parental species of grosbeaks having contrasting molt schedules relative to migration, suggesting high mortality costs to hybrids driven by molt biology, which are expressed later in life. Contrasts in molt schedules are absent in towhees. While migratory divides may exist for towhees and grosbeaks, the low adult survival of hybrid grosbeaks suggest that molt may be an important and underappreciated source of selection maintaining this and other narrow avian hybrid zones. 

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5. Genomic Architecture of Hybrid Male Sterility in a Species Without Sex Chromosomes ( Tigriopus californicus , Copepoda: Harpacticoida)

   https://doi.org/10.1093/gbe/evad091  

   Olsen, Kevin C; Lima, Thiago G; Barreto, Felipe S; Burton, Ronald S (June 2023, Genome Biology and Evolution)

   Katz, Laura A (Ed.)

   Abstract Sterility among hybrids is one of the most prevalent forms of reproductive isolation delineating species boundaries and is expressed disproportionately in heterogametic XY males. While hybrid male sterility (HMS) due to the “large X effect” is a well-recognized mechanism of reproductive isolation, it is less clear how HMS manifests in species that lack heteromorphic sex chromosomes. We evaluated differences in allele frequencies at approximately 460,000 SNPs between fertile and sterile F2 interpopulation male hybrids to characterize the genomic architecture of HMS in a species without sex chromosomes (Tigriopus californicus). We tested associations between HMS and mitochondrial-nuclear and/or nuclear-nuclear signatures of incompatibility. Genomic regions associated with HMS were concentrated on a single chromosome with the same primary 2-Mbp regions identified in one pair of reciprocal crosses. Gene Ontology analysis revealed that annotations associated with spermatogenesis were the most overrepresented within the implicated region, with nine protein-coding genes connected with this process found in the quantitative trait locus of chromosome 2. Our results indicate that a narrow genomic region was associated with the sterility of male hybrids in T. californicus and suggest that incompatibilities among select nuclear loci may replace the large X effect when sex chromosomes are absent. 

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