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The number of chromosomes varies tremendously across species. It is not clear whether having more or fewer chromosomes could be advantageous. The probability of non-disjunction should theoretically decrease with smaller karyotypes, but too long chromosomes should enforce spatial constraint for their segregation during the mitotic anaphase. Here, we propose a new experimental cell system to acquire novel insights into the mechanisms underlying chromosome segregation. We collected the endemic Australian ant Myrmecia croslandi, the only known species with the simplest possible karyotype of a single chromosome in the haploid males (and one pair of chromosomes in the diploid females), since males are typically haploid in hymenopteran insects. Five colonies, each with a queen and a few hundreds of workers, were collected in the Canberra district (Australia), underwent karyotype analysis to confirm the presence of a single pair of chromosomes in worker pupae, and were subsequently maintained in the laboratory in Paris (France). Starting from dissociated male embryos, we successfully conducted primary cell cultures comprised of single-chromosome cells. This could be developed into a unique model that will be of great interest for future genomic and cell biology studies related to mitosis.
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Hormigas , Cromosomas de Insectos , Animales , Hormigas/genética , Masculino , Femenino , Cultivo Primario de Células , Cariotipificación , Cariotipo , Haploidia , Segregación CromosómicaRESUMEN
Animals can be permanently attached to a substrate in terrestrial environments at certain stages of their development. Pupa adhesion has evolved multiple times in insects and is thought to maintain the animal in a place where it is not detectable by predators. Here, we investigate whether pupa adhesion in Drosophila can also protect the animal by preventing potential predators from detaching the pupa. We measured the adhesion of Drosophila species sampled from the same area and found that pupa adhesion varies among species, which can be explained by different glue production strategies. Then, we compared attached and manually detached pupae in both field and laboratory assays to investigate the role of pupa adhesion to prevent predation. First, we found that attached pupae remain onsite 30% more than detached pupae in the field after 3 days, probably because they are less predated. Second, we observed that attached pupae are less efficiently predated by ants in the laboratory: they are not carried back to the ant nest and more ants are needed to consume them onsite. Our results show that pupa adhesion can prevent the animal from being taken away by predators and is crucial for Drosophila fly survival.
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Hormigas , Conducta Predatoria , Animales , Drosophila , Insectos , PupaRESUMEN
Ants evolved about 140 million years ago and have diversified into more than 15,000 species with tremendous ecological and morphological diversity, yet evolution of the gene regulatory networks (GRNs) underlying this diversification remains poorly understood. Wing polyphenism, the ability of a single genome to produce either winged or wingless castes during development in response to environmental cues, is a nearly universal feature of ants. The underlying wing GRN is evolutionarily labile in worker castes of phylogenetically derived species: it is conserved in winged castes but interrupted at different points in wingless castes of different species. However, it remains unknown whether the wing GRN is interrupted in wingless castes of species from early branching lineages, and if so, whether it is interrupted at similar locations in worker castes of derived species. We therefore used in situ hybridization to assay the expression of nine genes in the wing GRN in wing imaginal discs of larvae from two species from the early branching ('basal') genus Mystrium. These species possess two castes each: Mystrium rogeri has winged queens and wingless workers, and M. oberthueri has wingless queens and wingless workers. In contrast to derived species, we found no evidence of interruption points in the wing GRN kernel of wingless castes. Our finding supports: (1) a "phylogenetic ladder model" of wing GRN evolution, where interruption points move further upstream in the wing GRN as ant lineages become more derived; and (2) that evolutionary lability of the GRN underlying wing polyphenism originated later during ant evolution.
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Hormigas/genética , Hormigas/fisiología , Evolución Biológica , Redes Reguladoras de Genes , Alas de Animales/anatomía & histología , Animales , Hormigas/anatomía & histología , Clonación Molecular , Regulación del Desarrollo de la Expresión GénicaRESUMEN
Warm temperatures decrease insect developmental time and body size. Social life could buffer external environmental variations, especially in large social groups, either through behavioral regulation and compensation or through specific nest architecture. Mean worker size and distribution of worker sizes within colonies are important parameters affecting colony productivity as worker size is linked to division of labor in insect societies. In this paper, we investigate the effect of stressful warm temperatures and the role of social environment (colony size and size of nestmate workers) on the mean size and size variation of laboratory-born workers in the small European ant Temnothorax nylanderi. To do so, we reared field-collected colonies under medium or warm temperature treatments after having marked the field-born workers and removed the brood except for 30 first instar larvae. Warm temperature resulted in the production of fewer workers and a higher adult mortality, confirming that this regime was stressful for the ants. T. nylanderi ants followed the temperature size rule observed in insects, with a decreased developmental time and mean size under warm condition. Social environment appeared to play an important role as we observed that (i) larger colonies buffered the effect of temperature better than smaller ones (ii) colonies with larger workers produced larger workers whatever the rearing temperature and (iii) the coefficient of variation of worker size was similar in the field and under medium laboratory temperature. This suggests that worker size variation is not primarily due to seasonal environmental fluctuations in the field. Finally, we observed a higher coefficient of variation of worker size under warm temperature. We propose that this results from a disruption of social regulation, i.e. the control of nestmate workers over developing larvae and adult worker size, under stressful conditions.
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Hormigas/anatomía & histología , Hormigas/fisiología , Tamaño Corporal/fisiología , Medio Social , Temperatura , AnimalesRESUMEN
The spectacular success of eusocial insects can be attributed to their sophisticated cooperation, yet cooperation is conspicuously absent during colony foundation when queens are alone. Selection against this solitary stage has led to a dramatically different strategy in thousands of eusocial insect species in which colonies are started by groups of nestmates and the benefits of sociality are retained continuously. Dependent colony foundation (DCF) evolved recurrently multiple times across the ants, bees, and wasps, though its prevalence in termites remains unclear. We review adaptations at both the colony level (reproductive investment shifts from sexuals to workers) and the individual level (wingless queens evolve in ants), and other consequences for life history (invasiveness, parasite transmission). Although few studies have focused on DCF, the accumulated data from anecdotal reports, supported by indirect information including morphology, population genetics, and colony demographics, make it clear that this strategy is more diverse and widespread than is usually recognized.
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Evolución Biológica , Himenópteros/fisiología , Isópteros/fisiología , Animales , Himenópteros/genética , Isópteros/genética , Comportamiento de Nidificación , Filogenia , Reproducción , Conducta SocialRESUMEN
Many ants have independently evolved castes with novel morphology as well as function, such as soldiers and permanently wingless (ergatoid) queens. We present a conceptual model, based on modularity in morphology and development, in which evolutionary innovation is facilitated by the ancestral ant polyphenism of winged queens and wingless workers. We suggest that novel castes evolved from rare intercastes, anomalous mosaics of winged queens and workers, erratically produced by colonies through environmental or genetic perturbations. The colonial environment is highly accommodating and buffers viable intercastes from individual selection. Their cost is limited because they are diluted by the large number of nestmates, yet some can bring disproportionate benefits to their colonies in the context of defense or reproduction (e.g., wingless intercastes able to mate). Useful intercastes will increase in frequency as their morphology is stabilized through genetic accommodation. We show that both soldiers and ergatoid queens are mosaics of winged queens and workers, and they are strikingly similar to some intercastes. Modularity and developmental plasticity together with winged/wingless polyphenism thus allow for the production of highly variable mosaic intercastes, and colonies incubate the advantageous mosaics.
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Hormigas/genética , Evolución Biológica , Modelos Genéticos , Animales , Hormigas/anatomía & histología , Femenino , Mosaicismo , Fenotipo , Selección Genética , Conducta SocialRESUMEN
BACKGROUND: Parasites cause predictable alternative phenotypes of host individuals. Investigating these parasitogenic phenotypes may be essential in cases where parasitism is common or taxa is described based on a parasitized individual. Ignoring them could lead to erroneous conclusions in biodiversity-focused research, taxonomy, evolution, and ecology. However, to date, integrating alternative phenotypes into a set of wild-type individuals in morphometric analysis poses extraordinary challenges to experts. This paper presents an approach for reconstructing the putative healthy morphology of parasitized ants using algorithmic processing. Our concept enables the integration of alternative parasitogenic phenotypes in morphometric analyses. METHODS: We tested the applicability of our strategy in a large pool of Cestoda-infected and healthy individuals of three Temnothorax ant species (T. nylanderi, T. sordidulus, and T. unifasciatus). We assessed the stability and convergence of morphological changes caused by parasitism across species. We used an artificial neural network-based multiclass classifier model to predict species based on morphological trait values and the presence of parasite infection. RESULTS: Infection causes predictable morphological changes in each species, although these changes proved to be species-specific. Therefore, integrating alternative parasitogenic phenotypes in morphometric analyses can be achieved at the species level, and a prior species hypothesis is required. CONCLUSION: Despite the above limitation, the concept is appropriate. Beyond parasitogenic phenotypes, our approach can also integrate morphometric data of an array of alternative phenotypes (subcastes in social insects, alternative morphs in polyphenic species, and alternative sexes in sexually dimorphic species) whose integrability had not been resolved before.
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Winter is a difficult period for animals that live in temperate zones. It can inflict high mortality or induce weight loss with potential consequences on performance during the growing season. Social groups include individuals of various ages and sizes. This diversity may improve the ability of groups to buffer winter disturbances such as starvation or cold temperature. Studies focusing on the buffering role of social traits such as mean size and diversity of group members under winter conditions are mainly performed in the laboratory and investigate the effect of starvation or cold separately. Here, we experimentally decreased worker size diversity and manipulated worker mean size within colonies in order to study the effect on overwintering survival in the ant Temnothorax nylanderi. Colonies were placed under natural conditions during winter. Colony survival was high during winter and similar in all treatments with no effect of worker size diversity and mean worker size. Higher brood survival was positively correlated with colony size (i.e., the number of workers). Our results show that the higher resistance of larger individuals against cold or starvation stresses observed in the laboratory does not directly translate into higher colony survival in the field. We discuss our results in the light of mechanisms that could explain the possible non-adaptive size diversity in social species.
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Trace metals such as cadmium are found in high concentrations in urban environments. Animal and plant populations living in heavily contaminated environments could adapt to trace metals exposure. A recent study shows that urban populations of the acorn ant Temnothorax nylanderi are more resistant to cadmium than their forest counterparts. However, this study was performed using field colonies that had just come out of hibernation. Because urban and forest hibernation environments differ, the differential resistance to trace metals may originate either from differential hibernation conditions or from a different resistance baseline to cadmium. In this study, we tested these two hypotheses using laboratory common garden hibernation conditions. We let urban and forest colonies of the ant T. nylanderi hibernate under the same laboratory conditions for four months. After this hibernation period, we also collected field-hibernating colonies and we compared cadmium resistance between urban and forest colonies depending on the hibernation condition. We found a differential response to cadmium under common garden, with urban colonies displaying less larval mortality and lower size reduction of the produced individuals. This suggests a different resistance baseline of urban colonies to cadmium. However, unexpectedly, we did not detect the differential response between urban and forest colonies in the field, suggesting a more complex scenario involving both genetic and environmental influences.
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Offspring quality and quantity are subject to a trade-off. Depending on species, ant colonies can produce either numerous winged queens that start new colonies alone (independent colony foundation [ICF]) or one propagule consisting of reproductives helped by workers (fission). Some species do both. In the Rhytidoponera impressa group, colonies with winged queens use ICF, whereas colonies with mated workers use fission. We assessed the effect of latitude and environment on colonial reproduction by collecting 79 colonies along the Australian east coast. A population dynamical model predicted that from tropical north to temperate south, seasonal fluctuations and harsher conditions should lead to a decrease in ICF success (-48%), making fission a suitable alternative. Yet, our empirical data showed that ICF persists at a higher rate than expected, presumably because it allows aerial dispersal, unlike fission. Investigation of colony demography and measurement of lean and fat weights in virgin winged queens and workers showed that, from north to south, colonies increase quality of queens relative to workers (+50%) at the cost of quantity (-86%). This modification limits the decrease in ICF success (-34%). A tremendous range of offspring phenotypes associated with quality-quantity trade-offs make ants competitive in diverse habitats.
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Hormigas/fisiología , Ecosistema , Temperatura , Clima Tropical , Animales , Conducta Animal , Peso Corporal/fisiología , Femenino , Masculino , Reproducción/fisiología , Conducta SocialRESUMEN
BACKGROUND: The origin of discrete novelties remains unclear. Some authors suggest that qualitative phenotypic changes may result from the reorganization of preexisting phenotypic traits during development (i.e., developmental recombination) following genetic or environmental changes. Because ants combine high modularity with extreme phenotypic plasticity (queen and worker castes), their diversified castes could have evolved by developmental recombination. We performed a quantitative morphometric study to investigate the developmental origins of novel phenotypes in the ant Mystrium rogeri, which occasionally produces anomalous 'intercastes.' Our analysis compared the variation of six morphological modules with body size using a large sample of intercastes. RESULTS: We confirmed that intercastes are conspicuous mosaics that recombine queen and worker modules. In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism. The six modules had distinct profiles of variation suggesting that each module responds differentially to factors that control body size and polyphenism. Mosaicism appears to result from each module responding differently yet in an ordered and predictable manner to intermediate levels of inducing factors that control polyphenism. The order of module response determines which mosaic combinations are produced. CONCLUSIONS: Because the frequency of mosaics and their canalization around a particular phenotype may evolve by selection on standing genetic variation that affects the plastic response (i.e., genetic accommodation), developmental recombination is likely to play an important role in the evolution of novel castes in ants. Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively. Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.
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INTRODUCTION: The mechanisms by which development favors or constrains the evolution of new phenotypes are incompletely understood. Polyphenic species may benefit from developmental plasticity not only regarding ecological advantages, but also potential for evolutionary diversification. For instance, the repeated evolution of novel castes in ants may have been facilitated by the existence of alternative queen and worker castes and their respective developmental programs. MATERIAL AND METHODS: Cataglyphis bombycina is exceptional in its genus because winged queens and size-polymorphic workers occur together with bigger individuals having saber-shaped mandibles. We measured seven body parts in more than 150 individuals to perform a morphometric analysis and assess the developmental origin of this novel phenotype. RESULTS: Adults with saber-shaped mandibles differ from both workers and queens regarding the size of most body parts. Their relative growth rates are identical to workers for some pairs of body parts, and identical to queens for other pairs of body parts; critical sizes differ in all cases. CONCLUSIONS: Big individuals are a third caste, i.e. soldiers, not major workers. Novel traits such as elongated mandibles are combined with a mix of queen and worker growth rates. We also reveal the existence of a dimorphism in the queen caste (microgynes and macrogynes). We discuss how novel phenotypes can evolve more readily in the context of an existing polyphenism. Both morphological traits and growth rules from existing queen and worker castes can be recombined, hence mosaic phenotypes are more likely to be viable. In C. bombycina, such a mosaic phenotype appears to function both for defense (saber-shaped mandibles) and fat storage (big abdomen). Recycling of developmental programs may have contributed to the morphological diversity and ecological success of ants.
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Hormigas/anatomía & histología , Hormigas/fisiología , Evolución Biológica , Animales , Femenino , Masculino , FenotipoRESUMEN
Recruitment in social insects often involves not only inducing nestmates to leave the nest, but also communicating crucial information about finding profitable food sources. Although bumblebees transmit chemosensory information (floral scent), the transmission mechanism is unknown as mouth-to-mouth fluid transfer (as in honeybees) does not occur. Because recruiting bumblebees release a pheromone in the nest that triggers foraging in previously inactive workers, we tested whether this pheromone helps workers learn currently rewarding floral odours, as found in food social learning in rats. We exposed colonies to artificial recruitment pheromone, paired with anise scent. The pheromone did not facilitate learning of floral scent. However, we found that releasing floral scent in the air of the colony was sufficient to trigger learning and that learning performance was improved when the chemosensory cue was provided in the nectar in honeypots; probably because it guarantees a tighter link between scent and reward, and possibly because gustatory cues are involved in addition to olfaction. Scent learning was maximal when anise-scented nectar was brought into the nest by demonstrator foragers, suggesting that previously unidentified cues provided by successful foragers play an important role in nestmates learning new floral odours.
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Abejas/fisiología , Flores , Odorantes , Alimentación Animal , Animales , Abejas/crecimiento & desarrollo , Conducta Alimentaria , Miel , Aprendizaje , Comportamiento de Nidificación , FeromonasRESUMEN
In ants, winged queens that are specialized for independent colony foundation can be replaced by wingless reproductives better adapted for colony fission. We studied this shift in reproductive strategy by comparing two Mystrium species from Madagascar using morphometry, allometry and dissections. Mystrium rogeri has a single dealate queen in each colony with a larger thorax than workers and similar mandibles that allow these queens to hunt during non-claustral foundation. In contrast, Mystrium 'red' lacks winged queens and half of the female adults belong to a wingless 'intermorph' caste smaller and allometrically distinct from the workers. Intermorphs have functional ovaries and spermatheca while those of workers are degenerate. Intermorphs care for brood and a few mate and reproduce making them an all-purpose caste that takes charge of both work and reproduction. However, their mandibles are reduced and inappropriate for hunting centipedes, unlike the workers' mandibles. This together with their small thorax disallow them to perform independent colony foundation, and colonies reproduce by fission. M. rogeri workers have mandibles polymorphic in size and shape, which allow for all tasks from brood care to hunting. In M. 'red', colonial investment in reproduction has shifted from producing expensive winged queens to more numerous helpers. M. 'red' intermorphs are the first case of reproductives smaller than workers in ants and illustrate their potential to diversify their caste system for better colonial economy.