Abstract
BackgroundA striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages.ResultsThe cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae.ConclusionsOur results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors.
Highlights
A striking aspect of evolution is that it often converges on similar trajectories
The current study examines convergent trait regression associated with the adoption of a cursorial lifestyle within the family Tetragnathidae, and asks whether changes in selection act on the same genes as in the related families of Mimetidae, Malkaridae, and Arkyidae, which are characterized by a similar adoption of a cursorial lifestyle and the absence of the aggregate/flagelliform triad [33]
The six assemblies recovered between 96.4 and 97.8% of the Benchmarking universal single copy orthologs (BUSCO) odb09 set of 1066 core arthropod genes, which is at the high end for de novo transcriptome assemblies and indicates good coverage of the protein-coding transcriptomes
Summary
A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Convergence is imposed by similar selective pressures across transitions to marine [5] or high altitude [6] environments, or with the adoption of phenotypes such as social behavior [7] and echolocation [8]. In these cases, convergence is associated with repeated gains of a suite of traits. In cases where similar phenotypes are displayed by distantly related taxa, to what extent can alternative genetic pathways operate to create similar suites of traits [13], and at what point in the formation of the phenotype [1]?
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