Adaptation of thermal scavenging ants to severe heat-conditions

Thermal scavenging is a unique behavior restricted to a few desert ant genera. Workers are among the most thermotolerant land animals known to this day, being able to survive body temperatures of sometimes more than 50°C for several minutes. Making use of their remarkable heat-hardiness, they search for food in plain day, a feat that other desert creatures cannot accomplish. They mostly feed on the corpses of heat-stricken, less tolerant arthropods that were unable to survive the blazing sun of the midday desert. Thermal scavenging has evolved independently at least three times in distantly related genera, geographical well segregated inside the different deserts of the world. First, the Cataglyphis genus ranges from the Sahara Desert and extends its distribution to reach minor Asia through the Mediterranean Basin. Second the Ocymyrmex genus can be found in the Namib and Karoo deserts of southern Africa, extending its range to eastern Africa savanna plains. Finally, the Melophorus genus can be found in Australia, with thermal scavenging species distributed in the central desert of the outback region.While this impressive behavior was already well-described by the start of this PhD project, little was known about the mechanisms supporting the remarkable heat-tolerance of workers. Using biophysical and physiological approaches in Cataglyphis and Ocymyrmex, we’ve been able to pinpoint key aspects underlying stress tolerance in those genera. First, from a biophysical standpoint, the Sahara silver ant Cataglyphis bombycina is covered with a unique and dense array of prismatic hairs reflecting visible wavelengths by total internal reflection. This allows reflection of up to 50% of the incident sunlight energy, thus shifting down the ant’s thermal equilibrium and sparing its body a few critical degrees. Second, in a comparative framework, we found numerous genes involved with critical cellular processes to be constitutively expressed or strongly up-regulated to heat in thermal scavenging ants, while their orthologs were not in mesophilic species. Those processes, such as molecular chaperoning, cell-cycle regulation, energy metabolism and muscular functions are keys that allow those ants to meet the higher requirement needed to scavenge for food at both stunning speed and under extreme heat-pressure. Overall, this work investigates the physiological and biophysical basis enabling thermal scavenging ants to survive extreme heat conditions. It provides a deeper understanding of cellular heat-tolerance pathways in non-model animals and contribute to our knowledge of life’s adaptation to extreme conditions.Doctorat en Sciencesinfo:eu-repo/semantics/nonPublishe

Proteome stability, heat hardening, and heat-shock protein expression profiles in Cataglyphis desert ants

In ectotherms, high temperatures impose physical limits, impeding activity. Exposure to high heat levels causes various deleterious and lethal effects, including protein misfolding and denaturation. Thermophilic ectotherms have evolved various ways to increase macromolecular stability and cope with elevated body temperatures; these include the high constitutive expression of molecular chaperones. In this study, we investigated the effect of moderate to severe heat shock (37-45°C) on survival, heat hardening, protein damage and the expression of five heat tolerance-related genes (hsc70-4 h1, hsc70-4 h2, hsp83, hsc70-5 and hsf1) in two closely related Cataglyphis ants that occur in distinct habitats. Our results show that the highly thermophilic Sahara ant Cataglyphis bombycina constitutively expresses HSC70 at higher levels, but has lower induced expression of heat tolerance-related genes in response to heat shock, as compared with the more mesophilic Cataglyphis mauritanica found in the Atlas Mountains. As a result, C. bombycina demonstrates increased protein stability when exposed to acute heat stress but is less disposed to acquiring induced thermotolerance via heat hardening. These results provide further insight into the evolutionary plasticity of the hsp gene expression system and subsequent physiological adaptations in thermophilous desert insects to adapt to harsh environmental conditions.SCOPUS: ar.jinfo:eu-repo/semantics/publishe

Total internal reflection :bright silver sheen and protection from solar radiation in the Saharan desert ant Cataglyphis bombycina (Formicidae).

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Cold comfort: metabolic rate and tolerance to low temperatures predict latitudinal distribution in ants

Metabolic compensation has been proposed as a mean for ectotherms to cope with colder climates. For example, under the metabolic cold adaptation and the metabolic homeostasis hypotheses (MCA and MHH), it has been formulated that cold-adapted ectotherms should display both higher (MCA) and more thermally sensitive (MHH) metabolic rates (MRs) at lower temperatures. However, whether such compensation can truly be associated with distribution, and whether it interplays with cold-tolerance to predict species’ climatic niches, remains largely unclear despite broad ecological implications thereof. Here, we teased apart the relationship between MRs, cold-tolerance, and distribution, to test the MCA/MHH among 13 European ant species. We report clear metabolic compensation effects, consistent with the MCA and MHH, where MR parameters strongly correlated with latitude and climatic factors across species’ distributions. The combination of both cold-tolerance and MR further upheld the best predictions of species’ environmental temperatures and limits of northernmost distribution. To our knowledge, this is the first study showing that the association of metabolic data with cold tolerance supports better predictive models of species’ climate and distribution in social insects than models including cold-tolerance alone. These results also highlight that adaptation to higher latitudes in ants involved adjustments of both cold-tolerance and MRs, to allow this extremely successful group of insects to thrive under colder climates.Metabolic compensation has been proposed as a mean for ectotherms to cope with colder climates. For example, under the metabolic cold adaptation and the metabolic homeostasis hypotheses (MCA and MHH), it has been formulated that cold-adapted ectotherms should display both higher (MCA) and more thermally sensitive (MHH) metabolic rates (MRs) at lower temperatures. However, whether such compensation can truly be associated with distribution, and whether it interplays with cold tolerance to predict species' climatic niches, remains largely unclear despite broad ecological implications thereof. Here, we teased apart the relationship between MRs, cold tolerance and distribution, to test the MCA/MHH among 13 European ant species. We report clear metabolic compensation effects, consistent with the MCA and MHH, where MR parameters strongly correlated with latitude and climatic factors across species' distributions. The combination of both cold tolerance and MRs further upheld the best predictions of species' environmental temperatures and limits of northernmost distribution. To our knowledge, this is the first study showing that the association of metabolic data with cold tolerance supports better predictive models of species' climate and distribution in social insects than models including cold tolerance alone. These results also highlight that adaptation to higher latitudes in ants involved adjustments of both cold tolerance and MRs, to allow this extremely successful group of insects to thrive under colder climates.</p

Total internal reflection accounts for the bright color of the saharan silver ant

The Saharan silver ant Cataglyphis bombycina is one of the terrestrial living organisms best adapted to tolerate high temperatures. It has recently been shown that the hairs covering the ant's dorsal body part are responsible for its silvery appearance. The hairs have a triangular cross-section with two corrugated surfaces allowing a high optical reflection in the visible and near-infrared (NIR) range of the spectrum while maximizing heat emissivity in the mid-infrared (MIR). Those two effects account for remarkable thermoregulatory properties, enabling the ant to maintain a lower thermal steady state and to cope with the high temperature of its natural habitat. In this paper, we further investigate how geometrical optical and high reflection properties account for the bright silver color of C. bombycina. Using optical ray-tracing models and attenuated total reflection (ATR) experiments, we show that, for a large range of incidence angles, total internal reflection (TIR) conditions are satisfied on the basal face of each hair for light entering and exiting through its upper faces. The reflection properties of the hairs are further enhanced by the presence of the corrugated surface, giving them an almost total specular reflectance for most incidence angles. We also show that hairs provide an almost 10-fold increase in light reflection, and we confirm experimentally that they are responsible for a lower internal body temperature under incident sunlight. Overall, this study improves our understanding of the optical mechanisms responsible for the silver color of C. bombycina and the remarkable thermoregulatory properties of the hair coat covering the ant's body.SCOPUS: ar.jinfo:eu-repo/semantics/publishe

Molecular chaperoning helps safeguarding mitochondrial integrity and motor functions in the Sahara silver ant Cataglyphis bombycina

The Sahara silver ant Cataglyphis bombycina is one of the world’s most thermotolerant animals. Workers forage for heat-stricken arthropods during the hottest part of the day, when temperatures exceed 50 °C. However, the physiological adaptations needed to cope with such harsh conditions remain poorly studied in this desert species. Using transcriptomics, we screened for the most heat-responsive transcripts of C. bombycina with aim to better characterize the molecular mechanisms involved with macromolecular stability and cell survival to heat-stress. We identified 67 strongly and consistently expressed transcripts, and we show evidences of both evolutionary selection and specific heat-induction of mitochondrial-related molecular chaperones that have not been documented in Formicidae so far. This indicates clear focus of the silver ant’s heat-shock response in preserving mitochondrial integrity and energy production. The joined induction of small heat-shock proteins likely depicts the higher requirement of this insect for proper motor function in response to extreme burst of heat-stresses. We discuss how those physiological adaptations may effectively help workers resist and survive the scorching heat and burning ground of the midday Sahara Desert.SCOPUS: ar.jinfo:eu-repo/semantics/publishe

Data for: Thermal limits of survival and reproduction depend on stress duration: a case study of <i>Drosophila suzukii</i>

&lt;p&gt;Data and code for &quot;Thermal limits of survival and reproduction depend on stress duration: a case study of &lt;em&gt;Drosophila suzukii&lt;/em&gt;&quot;. Contains three scripts with accompanying data for reproducing analyses and figures in the manuscript:&lt;/p&gt; &lt;ol&gt; &lt;li&gt;doseresponse_alltraits_bothsexes.R - uses data in &quot;alltraits_summary.xlsx&quot; to fit dose-response curves (Fig. 1) and calculate Lt&lt;sub&gt;50&nbsp;&lt;/sub&gt;for mortality or&nbsp;Et&lt;sub&gt;50&nbsp;&lt;/sub&gt;for coma, productivity, and sterility&lt;/li&gt; &lt;li&gt;coma_proxy_alltraits.R - uses data in &quot;all_data_long.xlsx&quot; to calculate proportions dead/alive, sterile/fertile and average productivity among early vs. late onset coma groups (Fig. 3)&lt;/li&gt; &lt;li&gt;microclimate_injury_accumulation.R - uses data in &quot;TDT_parameters&quot; (derived from Fig. 2 with data shown in Supporting Table 2) and modelled microclimate to estimate accumulated heat injury (per minute) for all traits across the year&nbsp;2018. On a representative summer day (Aug 5), injury accumulation during the day is shown in Fig. 4.&lt;/li&gt; &lt;/ol&gt; &lt;p&gt;For any inquiries or bugs, please contact Michael &Oslash;rsted ([email protected])&lt;/p&gt

Data for: Thermal limits of survival and reproduction depend on stress duration: a case study of <i>Drosophila suzukii</i>

&lt;p&gt;Data and code for &quot;Thermal limits of survival and reproduction depend on stress duration: a case study of &lt;em&gt;Drosophila suzukii&lt;/em&gt;&quot;. Contains three scripts with accompanying data for reproducing analyses and figures in the manuscript:&lt;/p&gt; &lt;ol&gt; &lt;li&gt;doseresponse_alltraits_bothsexes.R - uses data in &quot;alltraits_summary.xlsx&quot; to fit dose-response curves (Fig. 1) and calculate Lt&lt;sub&gt;50&nbsp;&lt;/sub&gt;for mortality or&nbsp;Et&lt;sub&gt;50&nbsp;&lt;/sub&gt;for coma, productivity, and sterility&lt;/li&gt; &lt;li&gt;coma_proxy_alltraits.R - uses data in &quot;all_data_long.xlsx&quot; to calculate proportions dead/alive, sterile/fertile and average productivity among early vs. late onset coma groups (Fig. 3)&lt;/li&gt; &lt;li&gt;microclimate_injury_accumulation.R - uses data in &quot;TDT_parameters&quot; (derived from Fig. 2 with data shown in Supporting Table 2) and modelled microclimate to estimate accumulated heat injury (per minute) for all traits across the year&nbsp;2018. On a representative summer day (Aug 5), injury accumulation during the day is shown in Fig. 4.&lt;/li&gt; &lt;/ol&gt; &lt;p&gt;For any inquiries or bugs, please contact Michael &Oslash;rsted ([email protected])&lt;/p&gt

Data for: Thermal limits of survival and reproduction depend on stress duration: a case study of <i>Drosophila suzukii</i>

Data and code for "Thermal limits of survival and reproduction depend on stress duration: a case study of Drosophila suzukii". Contains three scripts with accompanying data for reproducing analyses and figures in the manuscript: doseresponse_alltraits_bothsexes.R - uses data in "alltraits_summary.xlsx" to fit dose-response curves (Fig. 1) and calculate Lt50 for mortality or Et50 for coma, productivity, and sterility coma_proxy_alltraits.R - uses data in "all_data_long.xlsx" to calculate proportions dead/alive, sterile/fertile and average productivity among early vs. late onset coma groups (Fig. 3) microclimate_injury_accumulation.R - uses data in "TDT_parameters" (derived from Fig. 2 with data shown in Supporting Table 2) and modelled microclimate to estimate accumulated heat injury (per minute) for all traits across the year 2018. On a representative summer day (Aug 5), injury accumulation during the day is shown in Fig. 4. For any inquiries or bugs, please contact Michael Ørsted ([email protected]

Facing lethal temperatures: Heat‐shock response in desert and temperate ants

Abstract Global climate changes may cause profound effects on species adaptation, particularly in ectotherms for whom even moderate warmer temperatures can lead to disproportionate heat failure. Still, several organisms evolved to endure high desert temperatures. Here, we describe the thermal tolerance survival and the transcriptomic heat stress response of three genera of desert (Cataglyphis, Melophorus, and Ocymyrmex) and two of temperate ants (Formica and Myrmica) and explore convergent and specific adaptations. We found heat stress led to either a reactive or a constitutive response in desert ants: Cataglyphis holgerseni and Melophorus bagoti differentially regulated very few transcripts in response to heat (0.12% and 0.14%, respectively), while Cataglyphis bombycina and Ocymyrmex robustior responded with greater expression alterations (respectively affecting 0.6% and 1.53% of their transcriptomes). These two responsive mechanisms—reactive and constitutive—were related to individual thermal tolerance survival and convergently evolved in distinct desert ant genera. Moreover, in comparison with desert species, the two temperate ants differentially expressed thousands of transcripts more in response to heat stress (affecting 8% and 12.71% of F. fusca and Myr. sabuleti transcriptomes). In summary, we show that heat adaptation in thermophilic ants involved changes in the expression response. Overall, desert ants show reduced transcriptional alterations even when under high thermal stress, and their expression response may be either constitutive or reactive to temperature increase