Juvenile ecology drives adult morphology in two insect orders.

Peter T Rühr,Tilo Baumbach,Jörg U Hammel,Alexander Blanke,Melina Frenzel,Elena Borisova,Carina Edel,Fabian Wilde,Thomas Van De Kamp,Tomáš Faragó

doi:10.1098/rspb.2021.0616

Abstract

Most animals undergo ecological niche shifts between distinct life phases, but such shifts can result in adaptive conflicts of phenotypic traits. Metamorphosis can reduce these conflicts by breaking up trait correlations, allowing each life phase to independently adapt to its ecological niche. This process is called adaptive decoupling. It is, however, yet unknown to what extent adaptive decoupling is realized on a macroevolutionary scale in hemimetabolous insects and if the degree of adaptive decoupling is correlated with the strength of ontogenetic niche shifts. It is also unclear whether the degree of adaptive decoupling is correlated with phenotypic disparity. Here, we quantify nymphal and adult trait correlations in 219 species across the whole phylogeny of earwigs and stoneflies to test whether juvenile and adult traits are decoupled from each other. We demonstrate that adult head morphology is largely driven by nymphal ecology, and that adult head shape disparity has increased with stronger ontogenetic niche shifts in some stonefly lineages. Our findings implicate that the hemimetabolan metamorphosis in earwigs and stoneflies does not allow for high degrees of adaptive decoupling, and that high phenotypic disparity can even be realized when the evolution of distinct life phases is coupled.

Highlights

Species ecology can change dramatically during development [1,2], a process called ‘ontogenetic niche shift’ [3]
We demonstrate that adult head morphology is largely driven by nymphal ecology, and that adult head shape disparity has increased with stronger ontogenetic niche shifts in some stonefly lineages
If phenotypic traits are coupled between life phases, ontogenetic niche shifts may result in adaptive conflicts, because coupled traits cannot evolve independently according to divergent, life-phase-specific needs [2,4,5]

Summary

Background

Species ecology can change dramatically during development [1,2], a process called ‘ontogenetic niche shift’ [3]. Multivariate, phylogenetically corrected integration tests of the Procrustes-aligned shape data against the results of the principal coordinate analyses (PCoA) of ecological covariates show that the head shape of adult stoneflies is most strongly influenced by the feeding habits of their nymphs (R2 = 0.79, z = 3.91, p = 1e−4, n = 46), and not by feeding habits of the adults themselves (p = 0.41, n = 37; table 1; electronic supplementary material, table S9). Despite the strong ontogenetic niche shift resulting from the amphibiotic life style of stoneflies (figure 1; electronic supplementary material, tables S4 and S5), adult head and mandible morphology could not evolve independently from nymphal ecology. Low degrees of adaptive decoupling can still facilitate increased phenotypic disparity

Conclusion

Findings

18. Wollenberg Valero KC et al 2017 Transcriptomic and