Paul E. Marek and Wendy Moore

EVOLUTION

Significance

The enigmatic millipede Xystocheir bistipita has been rediscovered after a half-century. The rediscovery unexpectedly reveals that the species is bioluminescent. By reconstructing its evolutionary history, we show that X. bistipita is the evolutionary sister of Motyxia, the only bioluminescent millipede genus in the order Polydesmida. We demonstrate that bioluminescence originated in the group’s common ancestor and incrementally grew brighter through evolutionary time. Luminescence in Motyxia may have initially evolved to cope with metabolic stress triggered by a hot, dry environment and was repurposed as a warning signal by species colonizing high-elevation habitats with greater predation risk. The discovery of bioluminescence in X. bistipita and its pivotal evolutionary location provides insight into repeated evolution of bioluminescence across the tree of life.

Abstract

The rediscovery of the Californian millipede Xystocheir bistipita surprisingly reveals that the species is bioluminescent. Using molecular phylogenetics, we show that X. bistipita is the evolutionary sister group of Motyxia, the only genus of New World bioluminescent millipedes. We demonstrate that bioluminescence originated in the group’s most recent common ancestor and evolved by gradual, directional change through diversification. Because bioluminescence in Motyxia has been experimentally demonstrated to be aposematic, forewarning of the animal’s cyanide-based toxins, these results are contrary to aposematic theory and empirical evidence that a warning pattern cannot evolve gradually in unpalatable prey. However, gradual evolution of a warning pattern is plausible if faint light emission served another function and was co-opted as an aposematic signal later in the diversification of the genus. Luminescence in Motyxia stem-group taxa may have initially evolved to cope with reactive oxygen stress triggered by a hot, dry environment and was repurposed for aposematism by high-elevation crown-group taxa colonizing new habitats with varying levels of predation. The discovery of bioluminescence in X. bistipita and its pivotal phylogenetic location provides insight into the independent and repeated evolution of bioluminescence across the tree of life.

See: http://www.pnas.org/content/112/20/6419.abstract.html?etoc

PNAS May 19, 2015 vol. 112 no. 20 6419-6424

Fig. 1.

Bioluminescent millipedes: M. sequoiae (A and B) and M. bistipita (C and D). (Upper) Millipedes photographed under incident white light. (Lower) Millipedes photographed with light emitted from the cuticle. (Inset) A 5× magnification of the granular photocytes of M. bistipita. (Scale bars: 5.0 mm.)