Genomic Profiles of Diversification and Genotype–Phenotype Association in Island Nematode Lineages

Abstract

Understanding how new species form requires investigation of evolutionary forces that cause phenotypic and genotypic changes among populations. However, the mechanisms underlying speciation vary and little is known about whether genomes diversify in the same ways in parallel at the incipient scale. We address this using the nematode, Pristionchus pacificus, which resides at an interesting point on the speciation continuum (distinct evolutionary lineages without reproductive isolation), and inhabits heterogeneous environments subject to divergent environmental pressures. Using whole genome re-sequencing of 264 strains, we estimate FST to identify outlier regions of extraordinary differentiation (∼1.725 Mb of the 172.5 Mb genome). We find evidence for shared divergent genomic regions occurring at a higher frequency than expected by chance among populations of the same evolutionary lineage. We use allele frequency spectra to find that, among lineages, 53% of divergent regions are consistent with adaptive selection, whereas 24% and 23% of such regions suggest background selection and restricted gene flow, respectively. In contrast, among populations from the same lineage, similar proportions (34-48%) of divergent regions correspond to adaptive selection and restricted gene flow, whereas 13-22% suggest background selection. Because speciation often involves phenotypic and genomic divergence, we also evaluate phenotypic variation, focusing on pH tolerance, which we find is diverging in a manner corresponding to environmental differences among populations. Taking a genome-wide association approach, we functionally validate a significant genotype-phenotype association for this trait. Our results are consistent with P. pacificus undergoing heterogeneous genotypic and phenotypic diversification related to both evolutionary and environmental processes.

Adaptive genomic divergence under high gene flow between freshwater and brackish‐water ecotypes of prickly sculpin (Cottus asper) revealed by Pool‐Seq

“…In contrast, F ST outlier regions are not expected to deviate from a neutral allele frequency spectrum under the influence of locally restricted gene flow (Nachman & Payseur 2012). Similar to other studies (Feulner et al 2015;McGaughram et al 2016), we tested whether F ST outlier windows showed decreased T D (defined as lower 5% quantile of the genomewide average) and distinguished between (i) background selection (decreased T D in both habitats), (ii) directional selection with hitchhiking (decreased T D in one of both habitats), (iii) locally restricted gene flow (T D not decreased compared to genomewide average) and (iv) balancing selection (T D increased, p decreased).…”

“…; McGaughram et al . ), we tested whether F ST outlier windows showed decreased T D (defined as lower 5% quantile of the genomewide average) and distinguished between (i) background selection (decreased T D in both habitats), (ii) directional selection with hitchhiking (decreased T D in one of both habitats), (iii) locally restricted gene flow ( T D not decreased compared to genomewide average) and (iv) balancing selection ( T D increased, π decreased).…”

The search for loci under selection: trends, biases and progress

“…The targeted category includes methods that reduce the genome to areas that are more likely to include regions under selection, or target specific functional genes, and include transcriptomics‐based SNP detection (e.g., Limborg et al., ; Vangestel et al., ), SNP chip (Gunderson, Steemers, Lee, Mendoza, & Chee, ) and expressed sequence tags (EST; Bouck & Vision, ). Lastly, the census category includes only studies that use whole‐genome sequencing methods to obtain SNPs (e.g., McGaughran, ). We expected that library construction approaches that target functional gene regions ( targeted ) would identify a higher proportion of SNPs under selection than the other approaches.…”

Succession and dynamics of Pristionchus nematodes and their microbiome during decomposition of Oryctes borbonicus on La Réunion Island

“…Studies on La Réunion Island in the Indian Ocean revealed that P. pacificus has invaded this island multiple times independently with different carrier beetles, resulting in this island harboring the complete worldwide diversity of P. pacificus haplotypes (Herrmann et al ., ; Morgan et al ., ). Indeed, the population structure and evolutionary history of P. pacificus on La Réunion Island provided a paradigm for detailed studies of the nematodes´ adaptations to new environments (McGaughran et al ., ; 2014; ; Morgan et al ., ; Moreno et al ., ). Among several P. pacificus hosts on La Réunion, the endemic rhinoceros beetle Oryctes borbonicus represents an interesting study system because more than 90% of beetle individuals harbor P. pacificus dauer larvae (Morgan et al ., ).…”