Measuring the Costs of Limb Regeneration and Their Transgenerational Consequences in Two Nearctic Lady Beetles (Coleoptera: Coccinellidae)

Abstract

We examined the ability of Coleomegilla maculata DeGeer and Hippodamia convergens Guerin-Meneville to regenerate, during pupation, a foreleg amputated in the fourth instar. Leg regeneration was complete for 80.7% of amputated H. convergens larvae, with 12.5% regenerating partially, and 6.8% showing no regeneration. Regeneration in C. maculata was 72.2% complete, 20.5% partial, and 7.2% none, but mortality following ablation was slightly higher than for H. convergens (7.4 vs. 0.6%). Ablation/regeneration caused a slight delay in pupation, but pupation time, fresh mass at emergence, and reproductive performance remained unaffected in either species. Reciprocal crosses were made between regenerated and unoperated beetles, and 12 progeny reared from the second clutch of each female in all treatments. Mating treatment affected eclosion time in H. convergens, whereas in C. maculata, larval development and pupation time were also affected. Considering all treatments, larval mortality was higher in H. convergens than in C. maculata, but lower when both H. convergens parents regenerated. Parental mating treatment did not affect adult weight in either species, but development of C. maculata progeny was faster when only the sire regenerated, and slower when the only the dame regenerated, whereas progeny of regenerated sires completed pupated faster than those sired by controls. We infer that genes activated during regeneration have pleiotropic effects with subtle, gender-specific, epigenetic consequences. If these pleiotropic effects are genetically linked to important traits, regenerative genetic elements could be conserved in coccinellids via natural selection acting on these traits, rather than on regenerative ability per se.

Effect of larval thermal conditions on limb regeneration in a ladybird beetle, Cheilomenes sexmaculata

“…No significant difference was observed among the fresh BWs of amputated and unamputated adult beetles indicating the absence of tradeoff in BW with respect to regeneration. Similar results were found in other ladybird species: Hippodamia convergens Guérin‐Méneville and Coleomegilla maculata (DeGeer), where the regenerated adults showed no change in BW postemergence (Michaud, Abdelwahab, et al, 2020). Possibly, the beetle chose to compromise in the size of the regenerated appendage over BW.…”

“…Such reduction in the size of regenerated appendages has also been reported in mantids (Karuppanan, 1998), damselflies (Parvin & Cook, 1968), cockroaches (Tanaka et al, 1992), fishes (Mari‐Beffa et al, 1999), and amphibians and lizards (Fitch, 2003; Ritzman et al, 2012). While regeneration potential has clear advantages (Michaud, Abdelwahab, et al, 2020; Saxena et al, 2016; Wang et al, 2015), costs such as reduced limb size, delayed developmental duration (Saxena et al, 2016; Wu et al, 2019), reduced and disproportionate wings in stick insects (Maginnis, 2006b) have been reported. In previous studies on ladybird beetles, the ability to regenerate lost limbs is reported to be broadly conserved in 16 species including C. sexmaculata (Michaud, Nedved, et al, 2020).…”

“…The ability to regenerate lost appendages in ladybird beetles (Coleoptera: Coccinellidae) is a recently discovered phenomenon (Saxena et al, 2016; Wang et al, 2015; Zhou et al, 2021) and is reported to be broadly conserved in around 16 species of ladybird beetles (Michaud, Nedved, et al, 2020). In ladybird beetles, amputation of legs in immature stages leads to fully regenerated legs in adults (Michaud, Abdelwahab, et al, 2020, Michaud, Nedved, et al, 2020; Saxena et al, 2016; Wang et al, 2015) and followed by various tradeoffs including delayed development, altered body weight (BW), reproductive parameters (Abdelwahab et al, 2018; Saxena et al, 2016; Wang et al, 2015) and foraging capacity in adults (Bayoumy et al, 2019). Such physiological and behavioral responses are not exclusive to regeneration but are also seen in response to multiple biotic and abiotic conditions, such as food, photoperiod, temperature, and so forth.…”

“…In ladybird beetles, limb regeneration occurs during preadult stage (Michaud, Abdelwahab, et al, 2020; Saxena et al, 2016; Wang et al, 2015) and is an energy‐intensive physiological process (Maginnis, 2006a). Given the role of thermal experience of early immature stages in shaping adult morphology and physiology, it is likely that the same should hold true for regeneration.…”

Robustness in action: Leg loss does not affect mating success in male harvestmen

“…However, autotomy is often assumed to yield long-term consequences on fitness, as detached appendages or body parts often play a role in courtship, mating, or sperm transfer (reviewed in Emberts et al 2019). Evidence regarding the effects of autotomy on reproduction is equivocal nonetheless, as the loss of body parts is known to bring negative, neutral, or even positive effects to reproduction (Emberts et al 2019;Michaud et al 2020;Cirino et al 2021;García-Hernández and Machado 2021;Talavera et al 2021). For example, after 'tail' autotomy, female scorpions experienced decreased fecundity, whereas males did not experience decreases in mating success (García-Hernández and Machado 2021).…”