Flightlessness in insects enhances diversification and determines assemblage structure across whole communities

Abstract

Dispersal limitation has been recurrently suggested to shape both macroecological patterns and microevolutionary processes within invertebrates. However, because of potential interactions among biological, environmental, temporal, and spatial variables, causal links among flight-related traits, diversification and spatial patterns of community assembly remain elusive. Integrating genetic variation within species across whole insect assemblages, within a simplified spatial and environmental framework, can be used to reduce the impact of these potentially confounding variables. Here, we used standardized sampling and mitochondrial DNA sequencing for a whole-community characterization of the beetle fauna inhabiting a singular forested habitat (laurel forest) within an oceanic archipelago setting (Canary Islands). The spatial structure of species assemblages together with species-level genetic diversity was compared at the archipelago and island scales for 104 winged and 110 wingless beetle lineages. We found that wingless beetle lineages have: (i) smaller range sizes at the archipelago scale, (ii) lower representation in younger island communities, (iii) stronger population genetic structure, and (iv) greater spatial structuring of species assemblages between and within islands. Our results reveal that dispersal limitation is a fundamental trait driving diversity patterns at multiple hierarchical levels by promoting spatial diversification and affecting the spatial configuration of entire assemblages at both island and archipelago scales.

β diversity among ant communities on fragmented habitat islands: the roles of species trait, phylogeny and abundance

“…So, after a dispersal event of even a short distance, the ability of a queen to find a suitable nest site can be highly reduced. In addition, recent studies on butterflies and beetles – ants may have an intermediate dispersal ability between them – indicated that even short distances between islands and even intra‐island barriers can prevent dispersal and gene flow (Salces‐Castellano et al 2020, Scalercio et al 2020, Salces‐Castellano et al 2021). Thus, poor dispersers from the mainland might not reach remote islands, producing distance decay in β diversity as distance to nearest mainland increases.…”

Dispersal ability and its consequences for population genetic differentiation and diversification

“…Consistent with this, we find that population genetic structure in spiders and in beetles tends to be higher in non-dispersive lineages, at both archipelago and island scales, in line with similar findings from Salces-Castellano et al . [19]. Linear mixed models revealed a significant tendency for beetles but not for spiders.…”

“…To harmonize data with that of Salces-Castellano et al . [19], we adopted their approach by defining LMDHs, that minimize the probability of a given biological species being assigned to more than one LMDH, while simultaneously providing a similar time frame for comparisons among lineages. While mtDNA substitution rate variation may be expected across different spider lineages [33], there is no evidence that these should correlate with species dispersal ability.…”

“…Do the patterns observed by Salces-Castellano et al . [19] translate to a model of higher diversification when individual dispersal ability is limited (e.g. [16]), or a model where dispersal ability and diversification are uncoupled (e.g.…”

Digest: Dispersal reduction drives rapid diversification in alpine grasshoppers

“…Flight loss increases physical isolation among lineages and may increase the risk of extinction (Waters et al 2020). Yet, broad-scale analyses suggest that it may also be a key driver of insect diversification (Salces-Castellano et al 2021), though the demographic consequences of this evolutionary transition at the earliest stages of divergence remain poorly understood.…”