Phenology and the physiological niche are co‐adapted in a desert‐dwelling lizard

Flight of nocturnal insects may be limited by cool nighttime environmental temperatures. We used laboratory and field experiments to explore the thermal basis of nocturnal flight in wing‐polymorphic Gryllus lineaticeps crickets consisting of long‐winged (LW), flight‐capable morphs and short‐winged (SW), flight‐incapable morphs. These crickets are a model for life history evolution and loss of flight, but their thermal requirements for flight have been unknown. We hypothesized that LW crickets achieve warm body temperatures required for flight through a combination of behavioural thermoregulation, producing heat endogenously (either by initiating muscular thermogenesis or increasing resting metabolic rate) and minimizing heat loss (by circulatory adjustments or insulation). Summer evening air temperatures in the field gradually declined from 25 to 18°C during the hours of nighttime cricket activity. Laboratory LW crickets did not fly at a body temperature of 18°C, and 60% flew at 25°C. In an experimental thermal gradient, spontaneous flight did not occur until body temperature exceeded 35°C, confirming that nocturnal field air temperature limits flight in this species. In a thermal gradient, LW crickets preferred higher temperatures (~36°C) than SW crickets (~32.5°C). In the field, all crickets were warmer than air temperature but considerably cooler than their preferred temperatures. LW crickets had higher field body temperatures (24.3°C) than SW crickets (22.3°C). LW crickets spontaneously initiated muscular thermogenesis through wing vibrations, increasing body temperature to a pre‐flight maximum of 35°C. Muscular thermogenesis was limited below 25°C. LW crickets cooled more slowly and had higher metabolic rates than SW crickets. We conclude that LW crickets prepare to fly on cool nights by gaining heat from warm substrates, activating endogenous muscular thermogenesis and reducing their cooling rate. These mechanisms are absent or less pronounced in SW crickets. The overall thermoregulatory strategy we report represents a previously unrecognized component of insect dispersal polymorphism. We suggest that thermal constraints on nocturnal flight may have contributed to evolutionary loss of flight in other insect groups. A free Plain Language Summary can be found within the Supporting Information of this article.

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“…We multiplied by flow rate to get V CO 2 and V O 2 per min, expressed by mL g −1 min −1 (e.g. Lighton, 2018;Sun et al, 2018).…”

Section: Metabolic Modifications Hypothesismentioning

confidence: 99%

Nocturnal dispersal flight of crickets: Behavioural and physiological responses to cool environmental temperatures

et al. 2020

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“…Second, if a warming climate has negative effects on offspring as shown in some other lizards [ 42 , 43 ], then parents and offspring would perform worse overall in the warming climate than in the present climate. Third, if parents are capable of adjusting offspring phenotype via predictive adaptive plasticity, offspring would perform better in thermal environments similar to that of their parents, as suggested by the environmental matching hypothesis [ 25 , 48 – 51 ].…”

Section: Introductionmentioning

confidence: 99%

Anticipatory parental effects in a subtropical lizard in response to experimental warming

Sun

Wang

et al. 2018

Front Zool

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Parental effects may produce adaptive or maladaptive plasticity that either facilitates persistence or increases the extinction risk of species and populations in a changing climate. However, empirical evidence of transgenerational adaptive plastic responses to climate change is still scarce. Here we conducted thermal manipulation experiments with a factorial design in a Chinese lacertid lizard (Takydromus septentrionalis) to identify the fitness consequences of parental effects in response to climate warming. Compared to present climate conditions, a simulated warming climate significantly advanced the timing of oviposition, depressed the immune capability of post-partum females, and decreased the hatching success of embryos, but did not affect female reproductive output (clutch size and egg mass). These results indicate that maternal warming negatively affects female health, and embryonic hatchability. More interestingly, we found that offspring from parents exposed to warming environments survived well under a simulated warming climate, but not under a present climate scenario. Accordingly, our study demonstrates anticipatory parental effects in response to a warming climate in an ectothermic vertebrate. However, the fitness consequences of this parental effect will depend on future climate change scenarios.Electronic supplementary materialThe online version of this article (10.1186/s12983-018-0296-3) contains supplementary material, which is available to authorized users.

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“…However, previous studies have demonstrated that egg mass can vary seasonally and affect offspring phenotypes in this species (Sun et al . 2018) and other reptiles as well (Ji & Braña 2000; Du et al . 2014; Mitchell et al .…”

Section: Discussionmentioning

confidence: 99%

Phenotypic consequences of maternally selected nests: a cross‐fostering experiment in a desert lizard

Xia

Sun

et al. 2020

Integr. Zool.

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Despite the importance of maternally selected nests in shaping offspring phenotypes, our understanding of how the nest environment affects embryonic development and offspring traits of most non‐avian reptiles is rather limited largely due to the logistical difficulty in locating their nests. To identify the relative contributions of environmental (temporal [seasonal] and spatial [nest‐site]) and intrinsic (clutch) factors on embryonic development and offspring traits, we conducted a cross‐fostering experiment by swapping eggs between maternally‐selected nests of the toad‐headed agama (Phrynocephalus przewalskii) in the field. We found that nest environment explained a large proportion of variation in incubation duration, hatching success, and offspring size and growth. In contrast, clutch only explained a small proportion of variation in these embryonic and offspring traits. More significantly, compared with spatial effects, seasonal effects explained more phenotypic variation in both embryonic development and offspring traits. Eggs laid early in the nesting season had longer incubation durations and produced smaller hatchlings with higher post‐hatching growth rates than did later‐laid eggs. Consequently, hatchlings from early‐laid eggs reached larger body sizes prior to winter. In addition, we found that female toad‐headed agama did not select nests specific to reaction norms of their own offspring because hatchlings from original or translocated nests had similar phenotypic traits. Overall, our study demonstrates the importance of seasonal variation in nest environments in determining embryonic development and offspring phenotypes, which has not been widely appreciated at least in non‐avian reptiles.

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Phenology and the physiological niche are co‐adapted in a desert‐dwelling lizard

Cited by 21 publications

References 63 publications

Nocturnal dispersal flight of crickets: Behavioural and physiological responses to cool environmental temperatures

Nocturnal dispersal flight of crickets: Behavioural and physiological responses to cool environmental temperatures

Anticipatory parental effects in a subtropical lizard in response to experimental warming

Phenotypic consequences of maternally selected nests: a cross‐fostering experiment in a desert lizard

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