Genomics of Hybridization – Part 1

In a series of articles, I will discuss recent advances in hybridization genomics – the fundamentals of adaptive introgression, “islands of speciation”, differential gene flow, and linked selection have been discussed in my previous posts (here, here, and also at the Social Evolution Forum). I will focus this series on applications/support/fallibilities of theories in recent literature, and incidentally, also the focus of a new special issue of Molecular Ecology.
Hybridization following secondary contact in Myzomela honeyeaters – Sardell and Uy, 2016, Evolution

Studying a hybrid zone of Myzomela honeyeater songbirds (M. tristrami – sexually monochromatic, black, and M. cardinalis – sexually dichromatic, black and red) in the Solomon Islands, Sardell and Uy (2016) reveal a scenario of incomplete reproductive isolation, recent secondary contact, and their evolutionary consequences through analyses of nuclear and mitochondrial haplotypes of >200 birds sampled across six sites. One mitochondrial and six nuclear markers were then amplified, sequenced, and phased. Divergence time between the two species was then estimated using BEAST to be around 5.8 mya (95% CI: 3.1-9.3 mya). Hybridization was quantified by comparing identifying haplotypes present exclusively in allopatry in sympatric heterospecifics – showing exclusive mitochondrial introgression (sex biased), and nuclear introgression from M. cardinalis into M. tristrami. Both mitochondrial and nuclear diversities were larger in M. tristrami, indicative of larger effective population sizes. Similar admixture patterns were also determined using estimation of population structure. Further characterization of hybridization using more markers, and population genetic models in the species will reveal a better understanding of the genomics of hybrid zones

Maternal effects on gene expression Arabidopsis lyrata hybrids – Videvall et al. 2015, Molecular Biology and Evolution
With little knowledge of how hybridization affects fitness at the transcript level, Videvall et al. (2015) in a study of Scandinavian populations of the perennial herb, Arabidopsis lyrata use high-throughput RNAseq to quantify gene expression. Using lab generated hybrids of lowland coastal varieties from Sweden, and an alpine population in Norway, genome-wide expression was characterized in 26 seedlings, and compared in hybrids and progenitor populations. Significant differences were determined between expression levels in progeny derived solely from source populations, with larger variation within the Norwegian population (enhanced for genes involved in cell wall modification, and enzyme function) than in the Swedish population (enhanced for photosynthesis, metabolic processes). Hybrid gene expression levels were intermediate to both progenitor populations, and significantly more similar to maternal expression than paternal. This observation was true both across the genome, and for enhanced expression genes previously identified in source populations. No imprinting was detected by analyzing allele specific expression across 368 deep coverage SNP’s across transcripts. This experiment supports the additive parental model of gene expression in hybrids, with strong maternal effects, rather than dominance.

Most models of differentiation and speciation assume additive, dominance and/or epistatic genetic effects during outbreeding and hybridization, whereas the role of maternal effects is often neglected. Future tests of the adaptive significance of maternal effects during outbreeding and hybridization are expected to have important implications for understanding local adaptation and outbreeding depression in nature, and therefore for the general understanding of population differentiation and speciation.

Differential introgression detected using retrotransposons in wild wheats – Senerchia et al. 2015, Molecular Ecology
Wild wheats (Aegilops) are a diverse radiation of different ploidy level species across the Middle East, with spontaneous hybrids between the tetraploid Ae. geniculata and Ae. triuncialis being widely reported. Senerchia et al. (2015) use long-terminal repeat retrotransposons (LTR-RT’s) to determine their role in hybridization, and maintenance of species barriers in laboratory crosses, and 67 individuals sampled across natural hybrid zones in Israel. Lab crosses determined the spontaneous rate of hybridization to be 0.04% (0.01-0.15% 95% CI), sterile F1 males, and asymmetric postzygotic isolation with significantly more viable hybrids produced using Ae. triuncialis maternal parents. Using AFLP markers from six candidate LTR-RT’s and a k-means clustering algorithm, they obtained estimates of admixture, and proportions of new or lost loci during hybridization were quantified. 18.5 – 35.7% of individuals in the four sampling locations were classified to be introgressed, with preferential gene flow from Ae. geniculata into Ae. triuncialis. Comparison of variation around LTR-RT loci also revealed that these loci do not introgress in the same way as random sequences, indicative that they might be involved in maintaining species integrity in spite of introgression.
References:
Sardell, J.M. & Uy, J.A.C. Hybridization following recent secondary contact results in asymmetric genotypic and phenotypic introgression between island species of Myzomela honeyeaters. Evolution. DOI: 10.1111/evo.12864
Videvall, Elin, et al. “Strong maternal effects on gene expression in Arabidopsis lyrata hybrids.” Molecular biology and evolution (2015): msv342. DOI: 10.1093/molbev/msv342
Senerchia, Natacha, et al. “Differential introgression and reorganization of retrotransposons in hybrid zones between wild wheats.” Molecular ecology(2015). DOI: 10.1111/mec.13515