skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Diurnal temperature variation impacts energetics but not reproductive effort across seasons in a temperate dung beetle
Abstract Temperature varies on multiple timescales and ectotherms must adjust to these changes to survive. These adjustments may lead to energetic trade‐offs between self‐maintenance and reproductive investment. However, we know little about how diurnal and seasonal temperature changes impact energy allocation. Here we used a combination of empirical data and modeling of both thermoregulatory behaviors and body temperature to examine potential energetic trade‐offs in the dung beetleOnthophagus taurus. Beginning in March 2020, universities and laboratories were officially closed due to the COVID‐19 pandemic. We thus performed experiments at a private residence near Knoxville, Tennessee, USA, leveraging the heating, ventilation and air conditioning of the home to manipulate temperature and compare beetle responses to stable indoor temperatures versus variable outdoor temperatures. We collectedO. taurusbeetles in the early‐, mid‐, and late‐breeding seasons to examine energetics and reproductive output in relation to diurnal and seasonal temperature fluctuations. We recorded the mass of field fresh beetles before and after a 24‐h fast and used the resulting change in mass as a proxy for energetic costs of self‐maintenance across seasons. To understand the impacts of diurnal fluctuations on energy allocation, we held beetles either indoors or outdoors for 14‐day acclimation trials, fed them cow dung, and recorded mass change and reproductive output. Utilizing biophysical models, we integrated individual‐level biophysical characteristics, microhabitat‐specific performance, respirometry data, and thermoregulatory behaviors to predict temperature‐induced changes to the allocation of energy toward survival and reproduction. During 24 h of outdoor fasting, we found that beetles experiencing reduced temperature variation lost more mass than those experiencing greater temperature variation, and this was not affected by season. By contrast, during the 14‐day acclimation trials, we found that beetles experiencing reduced temperature variation (i.e., indoors) gained more mass than those experiencing greater temperature variation (i.e., outdoors). This effect may have been driven by shifts in the metabolism of the beetles during acclimation to increased temperature variation. Despite the negative relationship between temperature variation and energetic reserves, the only significant predictor of reproductive output was mean temperature. Taken together, we find that diurnal temperature fluctuations are important for driving energetics, but not reproductive output.  more » « less
Award ID(s):
2046368 1930829
PAR ID:
10542380
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Ecology
Date Published:
Journal Name:
Ecology
Volume:
105
Issue:
3
ISSN:
0012-9658
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Most studies exploring molecular and physiological responses to temperature have focused on constant temperature treatments. To gain a better understanding of the impacts of fluctuating temperatures, we investigated impacts of increased temperature variation on Phanaeus vindex dung beetles across levels of biological organization. Specifically, we hypothesized that increased temperature variation is energetically demanding. We predicted that thermal sensitivity of metabolic rate and energetic reserves would be reduced with increasing fluctuation. To test this, we examined responses of dung beetles exposed to constant (20°C), low fluctuation (20±5°C), or high fluctuation (20±12°C) temperature treatments using respirometry, energetic reserves, and HPLC-MS-based metabolomics. We found no significant differences in metabolic rates or energetic reserves, suggesting increased fluctuations were not energetically demanding. To understand why there was no effect of increased amplitude on energetics, we assembled and annotated a de novo transcriptome, finding non-overlapping transcriptomic and metabolomic responses of beetles exposed to different fluctuations. We found that 58 metabolites increased in abundance in both fluctuation treatments, but 15 only did so in response to high amplitude fluctuations. We found 120 transcripts were significantly upregulated following acclimation to any fluctuation, but 174 were upregulated only in beetles from the high amplitude fluctuation. Several differentially expressed transcripts were associated with post-translational modifications to histones that support a more open chromatin structure. Our results demonstrate that acclimation to different temperature fluctuations is distinct and may be supported by increasing transcriptional plasticity. Our results indicate for the first time that histone modifications may underlie rapid acclimation to temperature variation. 
    more » « less
  2. Invasive species may be more capable of adjusting to climate warming via phenotypic plasticity than native species since plasticity is thought to increase invasion success. Physiological plasticity via acclimation is one way in which organisms can adjust their thermal tolerance in response to temperature change, but few studies have addressed whether invasive species have greater thermal plasticity compared to native congeners. Here we investigated whether thermal plasticity via temperature acclimation varies between two Onthophagus dung beetle species, the non-native Onthophagus taurus and the native Onthophagus hecate, collected from both Florida and Tennessee, USA. We expected the non-native O. taurus to demonstrate greater plasticity than the native O. hecate; we also predicted that beetles from Florida would have reduced plasticity since their environment is less thermally variable. To examine thermal plasticity, we measured shifts in time until loss of function (i.e., leg mobility) following acclimation to hot or cold temperature treatments. We found that non-native O. taurus from Florida acclimated to warm temperatures, increasing time to loss of function following warm treatments; unexpectedly, O. taurus from Tennessee showed no warm acclimation ability. Onthophagus hecate did not acclimate to warm temperatures in either location. In contrast, both species showed similar levels of cold acclimation. Taken together, our results suggest that the non-native species, O. taurus, will be more capable of using physiological adjustments to respond to climate warming than the native species, O. hecate. 
    more » « less
  3. Duncan, Elizabeth J (Ed.)
    Phenotypic plasticity is thought to be an important driver of diversification and adaptation to environmental variation, yet the genomic mechanisms mediating plastic trait development and evolution remain poorly understood. The Scarabaeinae, or true dung beetles, are a species-rich clade of insects recognized for their highly diversified nutrition-responsive development including that of cephalic horns—evolutionarily novel, secondary sexual weapons that exhibit remarkable intra- and interspecific variation. Here, we investigate the evolutionary basis for horns as well as other key dung beetle traits via comparative genomic and developmental assays. We begin by presenting chromosome-level genome assemblies of three dung beetle species in the tribe Onthophagini (> 2500 extant species) includingOnthophagus taurus,O.sagittarius, andDigitonthophagus gazella. Comparing these assemblies to those of seven other species across the order Coleoptera identifies evolutionary changes in coding sequence associated with metabolic regulation of plasticity and metamorphosis. We then contrast chromatin accessibility in developing head horn tissues of high- and low-nutritionO.taurusmales and females and identify distinctcis-regulatory architectures underlying nutrition- compared to sex-responsive development, including a large proportion of recently evolved regulatory elements sensitive to horn morph determination. Binding motifs of known and new candidate transcription factors are enriched in these nutrition-responsive open chromatin regions. Our work highlights the importance of chromatin state regulation in mediating the development and evolution of plastic traits, demonstrates gene networks are highly evolvable transducers of environmental and genetic signals, and provides new reference-quality genomes for three species that will bolster future developmental, ecological, and evolutionary studies of this insect group. 
    more » « less
  4. Dung beetles, which move and bury the feces of vertebrates, are major drivers of ecosystem processes and provide crucial ecosystem services, including secondary seed dispersal. Dung beetles bury seed-containing dung in food caches or in brood balls used for breeding purposes, but little is known about how this behavior will be affected by climate change. We utilized field manipulations to investigate the effect of simulated climate change—including simultaneous increases in temperature mean and variance—on the seed dispersal behavior of two tunneling dung beetle species, Phanaeus vindex and Onthophagus taurus. We placed single adult females into either control or greenhouse treatments along with temperature loggers. We mixed glass beads of three sizes into cow dung to mimic seeds, provided beetles with the dung, and then allowed them to bury dung for either six or nine days. At the end of each trial, we recorded information on dung deposits, including the type (i.e., food cache or brood ball), number, size, burial depth, and the amount of each bead size found in the deposit. We found differences in burial depths of brood balls and food caches within species, as well as differences in the size and amount of beads buried between species. Exposure to higher temperatures resulted in brood balls being buried deeper across species, but did not change the burial depth of food caches. 
    more » « less
  5. Abstract Nutrition-dependent growth of sexual traits is a major contributor to phenotypic diversity, and a large body of research documents insulin signalling as a major regulator of nutritional plasticity. However, findings across studies raise the possibility that the role of individual components within the insulin signalling pathway diverges in function among traits and taxa. Here, we use RNAi-mediated transcript depletion in the gazelle dung beetle to investigate the functions of forkhead box O (Foxo) and two paralogs of the insulin receptor (InR1 and InR2) in shaping nutritional plasticity in polyphenic male head horns, exaggerated fore legs, and weakly nutrition-responsive genitalia. Our functional genetic manipulations led to three main findings: FoxoRNAi reduced the length of exaggerated head horns in large males, while neither InR1 nor InR2 knock-downs resulted in measurable horn phenotypes. These results are similar to those documented previously for another dung beetle (Onthophagus taurus), but in stark contrast to findings in rhinoceros beetles. Secondly, knockdown of Foxo, InR1, and InR2 led to an increase in the intercept or slope of the scaling relationship of genitalia size. These findings are in contrast even to results documented previously for O. taurus. Lastly, while FoxoRNAi reduces male forelegs in D. gazella and O. taurus, the effects of InR1 and InR2 knockdowns diverged across dung beetle species. Our results add to the growing body of literature indicating that despite insulin signalling's conserved role as a regulator of nutritional plasticity, the functions of its components may diversify among traits and species, potentially fuelling the evolution of scaling relationships. 
    more » « less