Serge Aron | Université libre de Bruxelles (original) (raw)

Papers by Serge Aron

Authorea (Authorea), Mar 10, 2021

Over the last decade, increasing attention has been paid to the molecular adaptations used by org... more Over the last decade, increasing attention has been paid to the molecular adaptations used by organisms to cope with thermal stress. However, to date, few studies have focused on thermophilic species living in hot, arid climates. In this study, we explored molecular adaptations to heat stress in the thermophilic ant genus Cataglyphis, one of the world's most thermotolerant animal taxa. We compared heat tolerance and gene expression patterns across six phylogenetically distant species that live in different habitats and experience different thermal regimes. We found that all six species had similar heat tolerance levels and critical thermal maxima. Furthermore, the transcriptome analyses revealed that, although the number of differentially expressed genes varied widely for the 6 species (from 54 to 1,118), many were also shared. Functional annotation of the differentially expressed and co-expressed genes then showed that the biological pathways involved in heat-shock responses were similar among species and were associated with four major processes: the regulation of transcriptional machinery and DNA metabolism; the preservation of proteome stability; the elimination of toxic residues; and the maintenance of cellular integrity. Overall, our results suggest that molecular responses to heat stress have been evolutionarily conserved in the ant genus Cataglyphis and that their versatility may help workers withstand temperatures close to their physiological limits.

Hybridization may help drive biological invasions by reducing Allee effects, increasing genetic v... more Hybridization may help drive biological invasions by reducing Allee effects, increasing genetic variation, and generating novel adaptive genotypes/phenotypes. Social insects (ants, bees, wasps, and termites) are among the world's worst invasive species. In this review, we study the relationship between hybridization and invasiveness in social insects. We examine three types of hybridization based on the reproductive characteristics of first-generation hybrids. We discuss several examples of the association between hybridization and invasiveness, which are predominantly found in bees and termites. However, hybridization also occurs in several noninvasive species, and highly invasive species are not consistently associated with hybridization events, indicating that hybridization is not a main driver of invasiveness in social insects. We discuss why hybridization is not more commonly seen in invasive social insects.

PLOS ONE, Sep 28, 2015

Each histogram shows the nuclear frequency with regard to DNA content for the head of a ... more Each histogram shows the nuclear frequency with regard to DNA content for the head of a single individual. The first peak corresponds to ploidy level, the second peak to nuclei with a double DNA content and the third peak to polyploid nuclei. In haploid males, the second peak (2C) corresponds to nuclei from mandibular muscles where cells are diploids.</p

bioRxiv (Cold Spring Harbor Laboratory), Jan 9, 2022

Aron (2022) Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphi... more Aron (2022) Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphis hispanica: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants, Peer Community Journal, 2: XX.

Molecular Ecology, Apr 25, 2003

The haplodiploid sex determining system in Hymenoptera, whereby males develop from haploid eggs a... more The haplodiploid sex determining system in Hymenoptera, whereby males develop from haploid eggs and females from diploid eggs, allows females to control the primary sex ratio (the proportion of each sex at oviposition) in response to ecological and /or genetic conditions. Surprisingly, primary sex ratio adjustment by queens in eusocial Hymenoptera has been poorly studied, because of difficulties in sexing the eggs laid. Here, we show that fluorescence in situ hybridization (FISH) can be used to accurately determine the sex (haploid or diploid) of eggs, and hence the primary sex ratio, in ants. We first isolated the homologue coding sequences of the abdominal-A gene from 10 species of 8 subfamilies of Formicidae. Our data show that the nucleotide sequence of this gene is highly conserved among the different subfamilies. Second, we used a sequence of 4.5 kbp from this gene as a DNA probe for primary sex ratio determination by FISH. Our results show that this DNA probe hybridizes successfully with its complementary DNA sequence in all ant species tested, and allows reliable determination of the sex of eggs. Our proposed method should greatly facilitate empirical tests of primary sex ratio in ants.

The Journal of Experimental Biology, Feb 1, 2023

ABSTRACT Over recent decades, increasing attention has been paid to how low-molecular-weight mole... more ABSTRACT Over recent decades, increasing attention has been paid to how low-molecular-weight molecules affect thermal tolerance in animals. Although the disaccharide sugar trehalose is known to serve as a thermal protectant in unicellular organisms, nothing is known about its potential role in insects. In this study, we investigated the effect of trehalose on heat tolerance in the Namib desert ant, Ocymyrmex robustior, one of the most thermotolerant animals found in terrestrial ecosystems. First, we tested whether a trehalose-supplemented diet increased worker survival following exposure to heat stress. Second, we assessed the degree of protein damage by comparing protein aggregation levels for trehalose-supplemented workers and control workers. Third, we compared the expression levels of three genes involved in trehalose metabolism. We found that trehalose supplementation significantly enhanced worker heat tolerance, increased metabolic levels of trehalose and reduced protein aggregation under conditions of heat stress. Expression levels of the three genes varied in a manner that was consistent with the maintenance of trehalose in the hemolymph and tissues under conditions of heat stress. Altogether, these results suggest that increased trehalose concentration may help protect Namib desert ant individuals against heat stress. More generally, they highlight the role played by sugar metabolites in boosting tolerance in extremophiles.

Peer Community Journal, Jul 18, 2022

Molecular Ecology Resources, Jun 28, 2008

We report the characterization of eight microsatellite markers in the bigheaded ant Pheidole mega... more We report the characterization of eight microsatellite markers in the bigheaded ant Pheidole megacephala, a pest ant registered in the list of '100 of the world's worst invasive alien species'. An enrichment protocol was used to isolate microsatellite loci, and polymorphism was explored with 36 individuals collected in an invasive population from Australia and 20 individuals collected in a population from the native mainland location in South Africa. These primers showed a number of alleles per locus ranging from two to 10, and expected heterozygosities ranging from 0.083 to 0.826. Moreover, results of cross-species amplification are reported in five other Pheidole species and in seven other ants of the subfamily Myrmicinae.

Biology Letters, Feb 1, 2015

We report a remarkable pattern of incongruence between nuclear and mitochondrial variations in a ... more We report a remarkable pattern of incongruence between nuclear and mitochondrial variations in a social insect, the desert ant Cataglyphis hispanica. This species reproduces by social hybridogenesis. In all populations, two distinct genetic lineages coexist; non-reproductive workers develop from hybrid crosses between the lineages, whereas reproductive offspring (males and new queens) are typically produced asexually by parthenogenesis. Genetic analyses based on nuclear markers revealed that the two lineages remain highly differentiated despite constant hybridization for worker production. Here, we show that, in contrast with nuclear DNA, mitochondrial DNA (mtDNA) does not recover the two lineages as monophyletic. Rather, mitochondrial haplotypes cluster according to their geographical origin. We argue that this cytonuclear incongruence stems from introgression of mtDNA among lineages, and review the mechanisms likely to explain this pattern under social hybridogenesis.

Scientific Reports, Dec 8, 2022

The reproductive division of labour is a hallmark of eusocial Hymenoptera. Females are either rep... more The reproductive division of labour is a hallmark of eusocial Hymenoptera. Females are either reproductive queens or non-reproductive workers. In ants, workers often display further task specialisation that is associated with variation in size and/or morphology. Because female polyphenism is typically under environmental control, it is thought epigenetic mechanisms (such as DNA methylation) play a central role since they mediate gene-by-environment interactions. Methylation of the growth-promoting gene epidermal growth factor receptor (egfr) was indeed shown to control worker size in a highly polymorphic ant. However, it remains unknown if egfr methylation could also regulate worker size in monomorphic species. By combining experimental pharmacology and molecular biology, we show that worker size is associated with egfr methylation in two monomorphic ants. Furthermore, we functionally demonstrate that EGFR signalling affects worker size. These results indicate that worker size regulation by egfr methylation has been mechanistically conserved in ants but remains unexploited in monomorphic species. Phenotypic plasticity occurs when a single genotype encodes multiple, diverse phenotypes 1. Common in all living organisms, it is often highly adaptive. By altering their phenotypes in response to external cues, organisms can react to environmental changes, boosting survival and reproduction. Some of the most remarkable forms of phenotypic plasticity are found in social Hymenoptera (bees, wasps, and ants) where the same genotype can lead to morphologically, physiologically, and behaviourally distinct female castes: large, fertile queens that specialise in reproduction, and smaller, usually sterile workers that ensure colony maintenance 2. Whether a female larva develops into a reproductive queen or a non-reproductive worker typically results from environmental (e.g., food quantity or quality) or social (e.g., queen and brood presence/absence) cues, which cause the baseline genome to express itself along different developmental lines 3-5. Unlike bees and wasps, numerous ant species exhibit a high degree of worker polymorphism, i.e. a colony's workers can vary in size and/or morphology 6,7. Worker size variation exists along a spectrum, ranging from monomorphism, where there are slight isometric differences, to dimorphism, where there are multiple, distinct worker subcastes that display marked, non-proportional differences in body features. Worker polymorphism has appeared repeatedly in Formicidae, suggesting that size-dependent division of labour in workers promotes colony fitness 8-10. Decades of research have been devoted to understanding the evolution and maintenance of worker polymorphism in ants. Yet, its genetic and developmental origins are only beginning to be deciphered. At the molecular level, body size is regulated by evolutionarily conserved growth-regulating pathways, such as the insulin/ insulin-like growth factor signalling (IIS) 11 , target of rapamycin (TOR) 12 , and epidermal growth factor receptor (EGFR) signalling 13. The pathways are triggered by dietary cues, causing cell-signalling cascades that promote cell growth, proliferation, and differentiation 14. In insects, the result is the production of the growth-regulating hormones ecdysone 15 and juvenile hormone (JH) 11,13,16. However, it remains unknown how these pathways have become fine-tuned to generate worker size variation from the same genotype. Recently, it has been hypothesised that epigenetic mechanisms, such as DNA methylation, are at play because they mediate gene-by-environment interactions, translating environmental signals into long-lasting changes in gene expression without modifying the DNA itself 17-19. Numerous studies have investigated whether DNA methylation influences queen-worker

Molecular Ecology Notes, Sep 1, 2003

Sex ratio variations during brood development have important implications for the study of sex al... more Sex ratio variations during brood development have important implications for the study of sex allocation in haplodiploid insects. So far, few studies have addressed this question because of the difficulty to determine the sex of the brood. We used flow cytometry to differentiate haploid males from diploid females in the ant Linepithema humile. Our data show that flow cytometry can be used successfully to distinguish between male and female brood on the basis of their DNA content, from the very first larval stage. Moreover, we show that flow cytometry allows sex brood determination in other ant species, as well as in nonsocial Hymenoptera.

PLOS ONE, Apr 13, 2016

(a) Reflectance. TIR is induced on the ant abdomen with an incident light at 50° and azi... more (a) Reflectance. TIR is induced on the ant abdomen with an incident light at 50° and azimuth 0. Reflectance is about 10-fold higher in the presence of hairs, for wavelengths ranging from 425 to 700 nm. (b) Heating curves. Abdomens are exposed for 90 seconds to the light emitted by a solar simulator whose visible spectral intensity is identical to the summer Saharan sun. Difference in excess temperature becomes significant after 45 seconds; after 90 seconds exposure, the difference in excess temperature between both conditions reaches 1.91°C. Unpaired Student t-test (*: p < 0.05, **: p < 0.01, ***: p < 0.001).</p

Bulletin de la Société royale des sciences de Liège, 2009

Social hybridogenesis has evolved repeatedly in ants (e.g., Pogonomyrmex, Solenopsis). Hybridogen... more Social hybridogenesis has evolved repeatedly in ants (e.g., Pogonomyrmex, Solenopsis). Hybridogenetic populations consist of self-sustainable pairs of hybridizing lineages. Queens of each pair mate with males of the opposite lineage to produce workers. By contrast, reproductive individuals arise from intra-lineage mating and maintain pure-lineage genomes. Recently, a new form of social hybridogenesis was discovered in the desert ant Cataglyphis hispanica. All workers are inter-lineage hybrids, whereas male and female sexuals are produced by asexual reproduction through parthenogenesis. As a consequence, only maternal genes should be perpetuated across generations. This system, as it stands, is expected to be evolutionarily short-lived due to long-term costs of asexual reproduction and selection against males, which do not contribute any genes to reproductive offspring. Contrary to this expectation, we show (i) that hybridogenetic lineages in Cataglyphis ants have been maintained over a long evolutionary time and across a large geographic scale. Hybridogenetic lineages occur in a whole complex of species that have diverged several millions years ago and are distributed from Northwest Africa to West Asia. (ii) Furthermore, a detailed survey of colonies structure in C. hispanica reveals that the workers are hybrids of the same two genetic lineages across the whole distribution range of the species. (iii) Remarkably, hybridogenetic Cataglyphis ants escape the costs of asexual reproduction by the sporadic production of new queens by intra-lineage mating, instead of parthenogenesis. Rare intra-lineage mated queens were found in polygynous colonies. Genetic analyses indicate that they lay fertilized eggs; these eggs fail to develop into workers but can achieve queen development. Thus, intra-lineage mated queens produce new queens and males only. Though they do not contribute to the production of the worker-force, these 'social parasites' promote genetic diversity and ensure non-null male fitness.

bioRxiv (Cold Spring Harbor Laboratory), Nov 12, 2022

Several genera of desert ants have adapted to endure prolonged exposure to high temperatures. The... more Several genera of desert ants have adapted to endure prolonged exposure to high temperatures. The study of these ants is essential to unravel how species respond and adapt to thermal stress. We investigated the thermal tolerance and the transcriptomic heat stress response of three desert ant genera (Cataglyphis, Melophorus and Ocymyrmex) and two temperate genera (Formica and Myrmica) to explore convergent and specific adaptations. We found a variable transcriptomic response among desert species exposed to similar levels of physiological heat-stress: Cataglyphis holgerseni and Melophorus bagoti differentially regulated very few transcripts, 0.12% (54/44,525) and 0.14% (53/38,726) respectively, while Cataglyphis bombycina and Ocymyrmex robustior showed greater expression alterations affecting 0.6% (253/41,912) and 1.53% (698/45,701) of their transcriptomes, respectively. These two responsive mechanisms-reactive and constitutive-were related to desert species thermal tolerance survival pattern and convergently evolved in distinct desert ant genera. By comparison, the two temperate species differentially expressed thousands of transcripts more than desert ants in response to heat stress (affecting 8% and 12,71% of F. fusca and Myr. sabuleti transcriptomes), suggesting that keeping restrained gene expression is an important adaptation in heat adapted species. Finally, we found a significant overlap of the molecular pathways activated in response to heat-stress in temperate and desert species, and our data revealed that larger gene expression responses also affected a greater number of taxonomically restricted genes. These results suggest that the molecular processes involved in heat-stress response are mostly evolutionary conserved in ants, but new genes may also play a role. .