Parallel evolution provides evidence for evolution by natural selection and can cause repeated divergence at specific genes. The parallel evolution of phenotypic traits under similar environmental pressures was estimated to cover almost half of same genomic regions. However, the genomic footprints of parallel evolution on parallel speciation is not clearly known yet. In a recent study, Víctor Soria-Carrasco et al. investigated the natural selection’s role in parallel speciation with stick insect populations.
Herbivorous stick insect (Timema cristinae) is an endemic species to California and adapted to different host plants, Adenostoma fasciculatum and Ceanothus spinosus. Researchers investigated the whole genome divergence by parallel speciation in a nice experimental set up with this species. T.cristinae individuals were sampled from four replicate population pairs where 3 of them were adjacent and one was 6.4 km far away. They annotated the reference genome for the species and resequenced 160 individuals sampled from field transplant experiment.
In the first part of the study, the data obtained was used to analyse the effects of adaptation on genomic divergence in different scales and aspects. The results showed that the divergence between ecotype pairs varied geographically. Principal components analysis and phylogenomic trees clustered the individuals by geography, not by host (Figure 1). Genome-wide fixation index was higher for the geographically separated population and lower for the adjacent populations. The genomic differentiation found in this study was lower than other studies that investigated the consequences of divergence. Afterwards, the researchers tested whether divergence between replicate population pairs frequently involved the same genomic regions by using the highly divergent single nucleotide polymorphisms (SNPs) between each population pair. The results showed that most of the SNPs (83%) were divergent only in one single population pair and divergence was non-parallel. The researchers discussed different evolutionary forces could gave rise to observed results. The remaining 17% of SNPs were represented in two or more population pairs and the pattern was in congruence with HMM.
In the second part of the study, the researchers performed a field transplant experiment. The design of the experiment let the researchers to maintain an “ancestor” population, a derived population hosted by Ceanothus and another by Adenostoma in 5 replicate blocks (Figure 3). The transplanted and “ancestor” insects were sampled after 1 year which corresponds to one generation of T.cristinae in nature. The genetic comparison between “ancestor” and transplanted individuals identified that most of the SNPs exhibit weak/moderate divergence. 213 SNPs exhibited larger allele frequency changes between hosts and were present in each block. ~15% of these SNPs were also supported by HMM and distributed across the genome.
Researchers examined the function of these genomic regions that might exhibit parallel divergence. The SNPs that pronounced as “parallel divergence SNPs” were present in four natural population pairs and located in the genes involved in metabolism and signal transduction (metal and calcium ion binding) pathways. They exhibited a 1.5-fold enrichment for being in coding regions of genes compared with all SNPs. Then, researchers performed the analysis for SNPs that were divergent between only a single population pair and also found the genes related to metal binding – non-parallel divergence? Researchers concluded these results as “(i)the result of adaptive divergence between host ecotypes, (ii) a case of parallelism at the functional level”.
Although some regions of the genome exhibited parallel divergence, the data showed that parallel speciation in Timema cristinae involve non-parallel genetic divergence.
Personal comments
The paper provides valuable information for speciation and annotation of the Timema cristinae genome will open new horizons. The sampling sites for the aim of the study are well planned and field transplant experiment is well designed. However, the paper is not so easy to read and follow because of massive background information. Also figures are not so helpful — I would not expect to see pie-charts between main figures. For example Figure2 and Figure 3, in which “quantification of parallel and nonparallel divergence across population pairs” and “allele frequency changes across the genome in a flied transplant experiment” was shown, are a bit redundant and can be in supplementary documents. Conversely, some figures in the supplementary material are worth to be in the paper since they help the reader to follow the story easily and visualise more valuable information than Figure 2 and Figure 3.
Nevertheless, this paper provides novel insights to the field and adds a genetic time-stamp on the complex process of speciation. I recommend reading this paper but allocating more time than usual to be able digest it.
Soria-Carrasco, V., Gompert, Z., Comeault, A., Farkas, T., Parchman, T., Johnston, J., Buerkle, C., Feder, J., Bast, J., Schwander, T., Egan, S., Crespi, B., & Nosil, P. (2014). Stick Insect Genomes Reveal Natural Selection’s Role in Parallel Speciation Science, 344 (6185), 738-742 DOI: 10.1126/science.1252136