Multiple paths towards repeated phenotypic evolution in the spiny-leg adaptive radiation (Tetragnatha; Hawaii)

Abstract

The repeated evolution of phenotypes is ubiquitous in nature and offers some of the clearest evidence of the role of natural selection in evolution. The genomic basis of repeated phenotypic evolution is often complex and can arise from a combination of gene flow, shared ancestral polymorphism and de novo mutation. Here, we investigate the genomic basis of repeated ecomorph evolution in the adaptive radiation of the Hawaiian spiny-leg Tetragnatha. This radiation comprises four ecomorphs that are microhabitat-specialists, and differ in body pigmentation and size (Green, Large Brown, Maroon, and Small Brown). Using 76 newly generated low-coverage, whole-genome resequencing samples, coupled with population genomic and phylogenomic tools, we studied the evolutionary history of the radiation to understand the evolution of the spiny-leg lineage and the genetic underpinnings of ecomorph evolution. Congruent with previous works, we find that each ecomorph has evolved twice, with the exception of the Small Brown ecomorph, which has evolved three times. The evolution of the Maroon and the Small Brown ecomorphs likely involved ancestral hybridization events, whereas the Green and the Large Brown ecomorphs likely evolved because of either standing genetic variation or de novo mutation. Pairwise comparisons of ecomorphs based on the fixation index (FST) show that divergent genomic regions include genes with functions associated with pigmentation (melanization), learning, neuronal and synapse activity, and circadian rhythms. These results show that the repeated evolution of ecomorphs in the Hawaiian spiny-leg Tetragnatha is linked to multiple genomic regions and suggests a previously unknown role of learning and circadian rhythms in ecomorph.

Consistent accumulation of transposable elements in species of the HawaiianTetragnathaspiny-leg adaptive radiation across the archipelago chronosequence

“…To compare TEs across individuals in our sample, we started by constructing a molecular phylogeny of the species in our data set. We examined this since there is evidence of hybridization in the spiny-leg radiation (Cerca et al ., 2023a), which can lead to topological differences in different datasets. First we cleaned the raw Illumina data by identifying and removing adapters using AdapterRemoval v2.3.2 (Schubert et al 2016).…”

“…Most lineages in the archipelago have colonized older islands, and progressed down the island chain as newer islands have formed (Shaw & Gillespie, 2016). The Tetragnatha spiny-leg spider radiation follows this colonization pattern from older to younger islands, which consists of 17 species that divergently evolved into one of four ecomorph types: “maroon”, “green”, “large brown”, and “small brown” (Gillespie, 1991, 2004; Roderick & Gillespie, 1998; Cerca et al ., 2023a). Since the radiation unfolds from older to younger islands, we can test whether the more recent colonization events on the younger islands correspond to an increase in TE accumulation.…”

Understanding natural selection and similarity: Convergent, parallel and repeated evolution

“…With the advent of massive genomic sequencing, there has been a growing interest in the general idea of ‘parallelism/convergence’ at the genome level, specifically, where mutations repeatedly arise on the genome (Martin & Orgogozo, 2013; Xie et al, 2019), where selection repeatedly acts (Bohutínská, Alston, et al 2021; Bohutínská, Vlček, et al, 2021; Kautt et al, 2012; Konečná et al, 2021; Poore et al, 2023; Rennison et al, 2019; Wos et al, 2021) and which genetic sources can lead to repeated evolution (Cerca et al, 2023; Lee & Coop, 2017; Montejo‐Kovacevich et al, 2022; Pease et al, 2016; Stern, 2013). As argued above, genotypic similarity does not necessarily result from natural selection, and distinctions between parallel and convergent evolution are prone to confusing interpretations due to the complexities of the processes at the genetic level, including the lack of one‐to‐one correspondence between the genotype and the phenotype or gene duplication events (see discussion associated with the second conceptual framework, above).…”

“…The advancements in genomic sequencing have significantly enhanced our understanding of the genetic sources contributing to similarity. Notably, the three identified sources of similarity are not mutually exclusive (Brown et al, 2019; Cerca et al, 2023; Konečná et al, 2021; Montejo‐Kovacevich et al, 2021; Natarajan et al, 2015; Pease et al, 2016; Signor et al, 2016). To distinguish between these sources, Lee and Coop (2017, 2019) developed a framework that combines haplotype‐based analysis and coalescence methods.…”

“…The advancements in genomic sequencing have significantly enhanced our understanding of the genetic sources contributing to similarity. Notably, the three identified sources of similarity are not mutually exclusive(Brown et al, 2019;Cerca et al, 2023;F I G U R E 3 (a)Different levels of biological organization at the genotypic level. (b) The three sources for the genetic basis include mutations, shared ancestral polymorphisms and gene flow.…”