Life-history specialization was not an evolutionary dead-end in Pyrenean cave beetles

Abstract

Research on subterranean organisms has focused on the colonization process and some of the associated phenotypic changes, but little is known on the longterm evolutionary dynamics of subterranean lineages and the origin of some highly specialized complex characters. One of the most extreme modifications is the reduction of the number of larval instars in some Leptodirini beetles from the ancestral 3 to 2 and ultimately a single instar. This reduction is usually assumed to have occurred independently multiple times within the same lineage and geographical area, but its evolution has never been studied in a phylogenetic framework. Using a comprehensive molecular phylogeny, we found a low number of independent origins of the reduction in the number of instars, with a single transition, dated to the Oligocene-Miocene, from 3 to 2 and then 1 instar in the Pyrenees, the best-studied area. In the Pyrenees, the 1-instar lineage had a diversification rate (0.22 diversification events per lineage per million years) significantly higher than that of 3-or 2-instar lineages (0.10), and similar to that seen in other Coleopteran radiations. Far from being evolutionary dead-ends, ancient lineages fully adapted to subterranean life seem able to persist and diversify over long evolutionary periods.

Developmental constraints in cave beetles

“…In this work, we analyse in detail the available data on the duration and size of the different developmental stages of subterranean leptodirine beetles in the phylogenetic context provided by Cieslak et al [10]. We find that the total duration of development is strongly conserved in these insects, despite variation in the number of instars and feeding behaviour of larvae; this developmental duration differs only in a clade of cave species from southeast France.…”

“…To place these species in a phylogenetic context, we used the phylogeny in [10], which includes 14 of these 15 species (the missing species is presumably related to another that is included) plus a comprehensive sampling of the main lineages of Leptodirini (electronic supplementary material).…”

“…We also find a strong correlation between first instar larval and adult body sizes, again regardless of number of larval moults. Both results suggest the presence of deeply conserved constraints in the timing and energy requirements of larval development, and at the same time higher variability in traits traditionally given greater biological relevance, such as the number of larval instars [9,10].…”

“…In the subterranean species of Leptodirini beetles, these modifications of larval development have been documented for several species in different geographical areas and have been traditionally assumed to have evolved multiple times independently, even in the case of closely related species [8,9]. However, with the use of a comprehensive molecular phylogeny, it has recently been shown that the number of independent origins of life cycle modification was low, with a single one in the Pyrenees, the geographical area for which most data are available [10]. In this lineage, there was a single transition during the Late Oligocene-Early Miocene from an ancestral 3-instar cycle [11] in species living in forest litter or under stones to a 2-instar cycle in species with fully subterranean habits (either in deep or shallow subterranean environments), in which the active larva still feeds.…”

“…In this lineage, there was a single transition during the Late Oligocene-Early Miocene from an ancestral 3-instar cycle [11] in species living in forest litter or under stones to a 2-instar cycle in species with fully subterranean habits (either in deep or shallow subterranean environments), in which the active larva still feeds. From within this lineage with a 2-instar cycle, there was then a single transition to a 1-instar, non-feeding larva in the Lower Miocene, in a lineage found today only in the deep subterranean environment of caves [10].…”