Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

Abstract

Interbreeding species often produce low‐fitness hybrids due to genetic incompatibilities between parental genomes. Whether these incompatibilities reflect fixed allelic differences between hybridizing species, or, alternatively, standing variants that segregate within them, remains unknown for many natural systems. Yet, evaluating these alternatives is important for understanding the origins and nature of species boundaries. We examined these alternatives using spadefoot toads (genus Spea), which naturally hybridize. Specifically, we contrasted patterns of gene expression in hybrids relative to pure‐species types in experimentally produced tadpoles from allopatric parents versus those from sympatric parents. We evaluated the prediction that segregating variation should result in gene expression differences between hybrids derived from sympatric parents versus hybrids derived from allopatric parents, and found that 24% of the transcriptome showed such differences. Our results further suggest that gene expression in hybrids has evolved in sympatry owing to evolutionary pressures associated with ongoing hybridization. Although we did not measure hybrid incompatibilities directly, we discuss the implications of our findings for understanding the nature of hybrid incompatibilities, how they might vary across populations over time, and the resulting effects on the evolutionary maintenance ‐ or breakdown ‐ of reproductive barriers between species.

Genome ofSpea multiplicata, a Rapidly Developing, Phenotypically Plastic, and Desert-Adapted Spadefoot Toad

“…multiplicata . To do this, we utilized previously generated RNA-seq data from tadpoles (Seidl et al 2019). RNA-seq reads were mapped to the assembly using Tophat2 v2.1.1 (Kim et al 2013).…”

Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression

“…The brain and liver were removed from three randomly selected tadpoles (out of five) per sibship among the three experimental conditions (n = 9 tadpoles for each of the six sibships). We extracted RNA and obtained measures of gene expression for a total of approximately 14 000 genes using 3 0 RNA-seq methods described in detail elsewhere [34,37,38], but additional details are provided in the electronic supplementary material.…”

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

“…Because gene expression is regulated through complex interactions of sequences and proteins within the cell, these interacting regulatory elements are thought to be co-adapted [ 40 ]. When these co-adapted complexes are disrupted, such as in hybrids, the regulatory targets may be mis-expressed, resulting in incompatibilities between species or divergent populations [ 39 , 41 ]. These incompatibilities are particularly likely to contribute to reproductive isolation when selection targets different components of a gene network [ 42 ], which can occur in replicate sympatric populations during cascade reinforcement.…”

“…In the only study of gene expression in a frog system undergoing reinforcement, the spadefoot toads ( Spea sp. ), Seidl et al [ 41 ] determined that divergence of gene expression profiles accompanies divergence of reproductive behaviors in sympatry. In spadefoots, the interacting species have evolved increased species discrimination within their contact zone, due to the negative consequences of hybridization [ 48 , 49 ] (but see [ 50 ]).…”

“…In spadefoots, the interacting species have evolved increased species discrimination within their contact zone, due to the negative consequences of hybridization [ 48 , 49 ] (but see [ 50 ]). Seidl et al [ 41 ] found that hybrids derived from interspecific crosses of parents originating in sympatry differed significantly in gene expression from their counterparts generated from allopatric parents. They concluded that ongoing hybridization in sympatry is driving the divergence of gene expression between geographic regions.…”