Beetle bioluminescence outshines extant aerial predators

Abstract

We understand very little about the timing and origins of bioluminescence, particularly as a predator avoidance strategy. Understanding the timing of its origins, however, can help elucidate the evolution of this ecologically important signal. Using fireflies, a prevalent bioluminescent group where bioluminescence primarily functions as aposematic and sexual signals, we explore the origins of this signal in the context of their potential predators. Divergence time estimations were performed using genomic-scale datasets providing a robust estimate for the origin of firefly bioluminescence as both a terrestrial and as an aerial signal. Our results recover the origin of terrestrial beetle bioluminescence at 141.17 (122.63–161.17) Ma and firefly aerial bioluminescence at 133.18 (117.86–152.47) Ma using a large dataset focused on Lampyridae; and terrestrial bioluminescence at 148.03 (130.12–166.80) Ma, with the age of aerial bioluminescence at 104.97 (99.00–120.90) Ma using a complementary Elateroidea dataset. These ages pre-date the origins of all known extant aerial predators (i.e. bats and birds) and support much older terrestrial predators (assassin bugs, frogs, ground beetles, lizards, snakes, hunting spiders and harvestmen) as the drivers of terrestrial bioluminescence in beetles. These ages also support the hypothesis that sexual signalling was probably the original function of this signal in aerial fireflies.

Rhagophthalmidae Olivier, 1907 (Coleoptera, Elateroidea): described genera and species, current problems, and prospects for the bioluminescent and paedomorphic beetle lineage

“…Within Coleoptera , bioluminescence can be found almost exclusively within the so-called “elaterid-lampyroid clade”, including Elateridae , Lampyridae , Phengodidae , Rhagophthalmidae , and Sinopyrophoridae , and probably the extinct Cretophengodidae ( Oba et al 2011 ; Fallon et al 2018 ; Bi et al 2019 ; Li et al 2021b ; Kusy et al 2021 ; Powell et al 2022 ). In Phengodidae , all known larvae and females are bioluminescent, as are males of some species ( Costa and Zaragoza-Caballero 2010 ).…”

“…]]; Oba (2015 : 99): bioluminescence; Amaral et al (2016 : 255): molecular phylogeny; Bocak et al (2016 : 2): molecular phylogeny; Kundrata et al (2016 : 293): molecular phylogeny; Lawrence (2016 : 17): classification; Wijekoon et al (2016 : 69): checklist [also as Rhagophthalminae ]; Amaral et al (2017a : 674): mitogenome, phylogeny; Kundrata et al (2017 : 153): molecular phylogeny; Martin et al (2017 : 564): phylogeny; Wang et al (2017 : 1): phylogeny; Yiu (2017 : 60): species descriptions, key; Bocak et al (2018 : 2): molecular phylogeny; Fallon et al (2018 : 2, 96): genomes, bioluminiscence; Kusy et al (2018a : 5): molecular phylogeny; Kusy et al (2018b : 2): molecular phylogeny; Tan (2018 : 127, 135): distribution, photographs; Zhang et al (2018 : 3): molecular phylogeny; Amaral et al (2019 : 283): molecular phylogeny [also as Rhagophtalmidae [sic! ]]; Chen et al (2019 : 4): molecular phylogeny; Jeng (2019 : 8): biofluorescence, biology; Kundrata et al (2019 : 1259): molecular phylogeny; Martin et al (2019 : 2): molecular phylogeny [also as Rhagophthalminae ]; McKenna et al (2019 : 4): molecular phylogeny; Liu et al (2020 : 46): luciferase, phylogeny [also as Rhagophthalminae ]; Rosa et al (2020 : 7): molecular phylogeny; Roza (2020 : 421): morphology, distribution; Zhang et al (2020 : 1): molecular phylogeny, bioluminescence; Douglas et al (2021 : 2): molecular phylogeny; Ge et al (2021 : 3): mitogenomic phylogeny; Kusy et al (2021 : 111): molecular phylogeny; Li et al (2021a : 5): remark; Li et al (2021b : 1): phylogeny, distribution, morphology; Seri and Rahman (2021 : 715): remark; Cai et al (2022 : 6): molecular phylogeny; Ge et al (2022 : 2): mitogenomic phylogeny; Powell et al (2022 : 1): molecular phylogeny, bioluminescence [also as Rhagophtalmidae [sic!]]. In addit...…”

Behavioral responses of bioluminescent fireflies to artificial light at night

“…For firefly adults, bioluminescence is a main component of a multimodal aposematic signal that is also thought to include reflectancebased red, yellow, and black warning coloration (Stevens and Ruxton, 2012), wing beat frequencies (Leavell et al, 2018), and ultrasonic clicks (Krivoruchko et al, 2021). Firefly larvae employ bioluminescence exclusively as an aposematic signal, in combination with warning coloration (De Cock and Matthysen, 2001), and likely have done so for close to 150 million years (Martin et al, 2017;Powell et al, 2022). By interfering with the detection of these reflectance-and emission-based visual signals of unpalatability, ALAN has the potential to heighten predation on firefly adults and larvae (Briolat et al, 2021).…”

“…Worldwide, over 2200 species of firefly and glow-worm beetles (family Lampyridae, hereafter referred to collectively as fireflies), are currently described (Martin et al, 2019). All firefly species bioluminesce in their larval stage, an adaptation which presumably originated to warn predators of their unpalatable chemical defenses (Branham and Wenzel, 2003;Powell et al, 2022; but note Kok et al, 2019). Most species subsequently coopted this ability to produce both aposematic signals and sexual advertisements during their brief adult stage (Leavell et al, 2018).…”

Similar enzymatic functions in distinct bioluminescence systems: Evolutionary recruitment of sulfotransferases in ostracod light organs

“…Although fireflies, sea pansies, and cypridinid ostracods convergently evolved the same mechanism for luciferin sulfation, the extent of evolutionary convergence varies across levels of biological organization. These taxa convergently evolved bioluminescence as a defense mechanism -which was later co-opted for courtship in fireflies (Powell et al 2022) and ostracods (Ellis et al 2022) -but produce light by using structurally diverse organs or tissue (Peterson and Buck 1968;Spurlock and Cormier 1975;Huvard 1993), different luciferins (Tsarkova 2021), and non-homologous luciferases (Cormier and Kazuo 1964;Oba et al 2003;Oakley 2005) (Figure 1). Understanding how these taxa genetically encode luciferin sulfation and synthesizing these findings with those from other levels of biological organization -namely, organismal, organ, and tissue -will reveal the extent to which convergently evolved phenotypes may vary across levels of biological organization.…”