Predatory fireflies and their toxic firefly prey have evolved distinct toxin resistance strategies

Yang, Lu; Borne, Flora; Betz, Anja; Aardema, Matthew L.; Zhen, Ying; Peng, Julie; Visconti, Regina; Wu, Mariana; Roland, Bartholomew P.; Talsma, Aaron D.; Palladino, Michael J.; Petschenka, Georg; Andolfatto, Peter

doi:10.1016/j.cub.2023.10.063

Cited by 8 publications

(4 citation statements)

References 59 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Parallel evolution of ATPα target-site insensitivity has been reported in multiple CTS-resistant insects ( 54–56 ). Recent study has also reported that ATPα target-site insensitivity plays important roles in CTS resistance in Photuris and Photinus fireflies ( 57 ). ATPα across Lampyridae is highly conserved, with at least 91% amino acid identity.…”

Section: Resultsmentioning

confidence: 98%

See 1 more Smart Citation

Firefly toxin lucibufagins evolved after the origin of bioluminescence

Zhu,

Lu,

Cai

et al. 2024

PNAS Nexus

Self Cite

View full text Add to dashboard Cite

Fireflies were believed to originally evolve their novel bioluminescence as warning signals to advertise their toxicity to predators, which was later adopted in adult mating. Although the evolution of bioluminescence has been investigated extensively, the warning signal hypothesis of its origin has not been tested. In this study, we test this hypothesis by systematically determining the presence or absence of firefly toxin lucibufagins (LBGs) across firefly species and inferring the time of origin of LBGs. We confirm the presence of LBGs in the subfamily Lampyrinae, but more importantly, we reveal the absence of LBGs in other lineages, including the subfamilies of Luciolinae, Ototretinae, and Psilocladinae, two incertae sedis lineages, and the Rhagophthalmidae family. Ancestral state reconstructions for LBGs based on firefly phylogeny constructed using genomic data suggest that the presence of LBGs in the common ancestor of the Lampyrinae subfamily is highly supported but unsupported in more ancient nodes, including firefly common ancestors. Our results suggest that firefly LBGs probably evolved much later than the evolution of bioluminescence. We thus conclude that firefly bioluminescence did not originally evolve as direct warning signals for toxic LBGs and advise that future studies should focus on other hypotheses. Moreover, LBG toxins are known to directly target and inhibit the α subunit of Na+, K+-ATPase (ATPα). We further examine the effects of amino acid substitutions in firefly ATPα on its interactions with LBGs. We find that ATPα in LBG-containing fireflies is relatively insensitive to LBGs, which suggests that target-site insensitivity contributes to LBG-containing fireflies' ability to deal with their own toxins.

show abstract

Section: Resultsmentioning

confidence: 98%

“…4 F). Photuris species evolved LBG resistance independently under distinct ecological contexts and were thoroughly investigated in a separate study ( 57 ).…”

Section: Resultsmentioning

confidence: 99%

Firefly toxin lucibufagins evolved after the origin of bioluminescence

Zhu,

Lu,

Cai

et al. 2024

PNAS Nexus

Self Cite

View full text Add to dashboard Cite

show abstract

“…In general, toxin-sequestering animals often have specialized mechanisms of toxin resistance when compared to non-toxic relatives [31]. For example, three amino acid replacements in the ATPα protein evolved in association with cardenolide sequestration in Danainae butterflies [36,37] and predatory fireflies that sequester lucibufagins have ATPα gene duplications that enhance lucibufagin resistance [38].…”

Section: Resultsmentioning

confidence: 99%

Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses

Tarvin,

Coleman,

Donoso

et al. 2024

Preprint

View full text Add to dashboard Cite

Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Further, we confirm the presence of alkaloids in two putatively non-toxic frogs from other families. Our data suggest the existence of a phenotypic intermediate between toxin consumption and sequestration - passive accumulation - that differs from active sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms.

show abstract

“…These studies led the most important researcher of Photurinae and femme fatale behavior, the late Prof. James Lloyd, to think that femmes fatales are the source of selective pressures that have been crucial for the evolutionary divergence of bioluminescent signals in prey firefly species of the American continent ( [15]; see also [12,15,17,18]). Females of predatory Photuris have morphological adaptations apparently designed to subdue and consume their prey [19], and recent molecular studies have identified genes involved in resistance to lucibufagins [20] and several candidate genes that could represent diverse physiological adaptations for the consumption of potentially toxic prey [21]. Thus, it is expected that Photuris predation is the source of selective pressures promoting the evolution of countermeasures in their prey fireflies [15,18], which resulted in a coevolutionary process that could be responsible for the complexity and plasticity frequently observed in the communication systems of fireflies [12,16,18,[22][23][24][25][26].…”

Section: Introductionmentioning

confidence: 99%

Deceptive Seduction by Femme Fatale Fireflies and Its Avoidance by Males of a Synchronous Firefly Species (Coleoptera: Lampyridae)

Maquitico,

Coronado,

Luna

et al. 2024

Insects

View full text Add to dashboard Cite

Photuris female fireflies attract males of different firefly species by responding to their flashing signals; then, they try to capture and feed on them. This aggressive mimicry is considered a major selective pressure on the communication systems of the fireflies of the American continent. The intensity of this selective pressure is a function of its efficiency in prey capture. In this study, the rates of attraction and capture of males of the synchronous firefly Photinus palaciosi by the predatory females of Photuris lugubris are reported. Although the females attract numerous males, their hunting success is low. This result is consistent with the few previous measurements published. In agreement with the predicted coevolutionary race between predator and prey, behaviors consistent with predation avoidance in P. palaciosi and increasing prey encounters and prey deception by P. lugubris were observed.

show abstract

Predatory fireflies and their toxic firefly prey have evolved distinct toxin resistance strategies

Cited by 8 publications

References 59 publications

Firefly toxin lucibufagins evolved after the origin of bioluminescence

Firefly toxin lucibufagins evolved after the origin of bioluminescence

Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses

Deceptive Seduction by Femme Fatale Fireflies and Its Avoidance by Males of a Synchronous Firefly Species (Coleoptera: Lampyridae)

Contact Info

Product

Resources

About