Belgica Antarctica Research Articles

Thermal responses of the embryos and early instar larvae of the Antarctic midge Belgica antarctica (Insecta: Diptera)

Thermal responses of the embryos and early instar larvae of the Antarctic midge Belgica antarctica (Insecta: Diptera)

Genetic history, structure and gene flow among populations of Belgica antarctica, the only free-living insect in the western Antarctic Peninsula

Changes in climate and environment can impact the sustainability of populations and biodiversity. Understanding population genetic diversity in the past and present can help us better predict species' responses to future environmental change. Antarctica has experienced drastic environmental change which threatens its biodiversity. In this study, we characterized the phylogeography and population genetic structure of Belgica antarctica, a wingless midge that is endemic to the western Antarctic Peninsula. This insect has adaptive features to withstand extremes in temperature, salinity, humidity, anoxia and pH. Belgica antarctica is widespread on widely dispersed islands of ice-free habitat, but questions remain regarding its genetic history, diversity and gene flow. We created nuclear-based, single nucleotide polymorphism (SNP) markers and genotyped 229 individuals from 11 populations to examine historical and current population genetic patterns. Our results support recent divergence among populations on different islands within the last 1 Mya. Furthermore, despite a lack of wings, B. antarctica exhibited frequent migration among islands, perhaps via ocean currents or phoresy with Antarctic vertebrates (e.g. seabirds). The close link between the evolutionary history of B. antarctica and the region's environment and ecology emphasize the importance of understanding its population dynamics to predict its persistence under environmental change.

Gene family expansions in Antarctic winged midge as a strategy for adaptation to cold environments

Parochlus steinenii is the only flying insect native to Antarctica. To elucidate the molecular mechanisms underlying its adaptation to cold environments, we conducted comparative genomic analyses of P. steinenii and closely related lineages. In an analysis of gene family evolution, 68 rapidly evolving gene families, involved in the innate immune system, unfolded protein response, DNA packaging, protein folding, and unsaturated fatty acid biosynthesis were detected. Some gene families were P. steinenii-specific and showed phylogenetic instability. Acyl-CoA delta desaturase and heat shock cognate protein 70 (Hsc70) were representative gene families, showing signatures of positive selection with multiple gene duplication events. Acyl-CoA delta desaturases may play pivotal roles in membrane fluidity, and expanded Hsc70 genes may function as chaperones or thermal sensors in cold environments. These findings suggest that multiple gene family expansions contributed to the adaptation of P. steinenii to cold environments.

Unsupervised learning for detection of possible sexual dimorphism in larvae of Belgica antarctica Jacobs (Diptera, Chironomidae)

Belgica antarctica is one of the two native chironomid species of the Antarctic Peninsula. In this species, adult males and females are considerably different, yet the question of larval sex differences in morphometric parameters remains unanswered. In this paper, we analyze five morphometric parameters: head capsule length, head capsule width, mandible width, mandible length, mentum length of 140 fourth-instar larvae of B. antarctica from seven study plots in the south of Petermann Island, Wilhelm Archipelago, Antarctic Peninsula. To infer possible sexual dimorphism, we use the methods of unsupervised analysis (PCA and hierarchical clusterization). Our results suggest that the selected morphometric features of width and length are highly intercorrelated and cannot differentiate sex in the sampled larvae of B. antarctica.

Simulated winter warming negatively impacts survival of Antarctica's only endemic insect

Abstract Antarctic winters are challenging for terrestrial invertebrates, and species that live there have specialised adaptations to conserve energy and protect against cold injury in the winter. However, rapidly occurring climate change in these regions will increase the unpredictability of winter conditions, and there is currently a dearth of knowledge on how the highly adapted invertebrates of Antarctica will respond to changes in winter temperatures. We evaluated the response of larvae of the Antarctic midge, Belgica antarctica, to simulated winters at three ecologically relevant mean temperature scenarios: warm (−1°C), normal (−3°C) and cold (−5°C). Within each scenario, larvae were placed into three distinct habitat types in which they are commonly observed (decaying organic matter, living moss, and Prasiola crispa algae). Following the simulated overwintering period, a range of physiological outcomes were measured, namely survival, locomotor activity, tissue damage, energy store levels and molecular stress responses. Survival, energy stores and locomotor activity were significantly lower following the Warm overwintering environment than at lower temperatures, but tissue damage and heat shock protein expression (a proxy for protein damage) did not significantly differ between the three temperatures. Survival was also significantly lower in larvae overwintered in Prasiola crispa algae, although the underlying mechanism is unclear. Heat shock proteins were expressed least in larvae overwintering in living moss, suggesting it is less stressful to overwinter in this substrate, perhaps due to a more defined structure affording less direct contact with ice. Our results demonstrate that a realistic 2°C increase in winter microhabitat temperature reduces survival and causes energy deficits that have implications for subsequent development and reproduction. While our Warm winter scenario was close to the range of observed overwintering temperatures for this species, warmer winters are expected to become more common in response to climate change. Conversely, if climate change reduces the length of winter, some of the negative consequences of winter warming may be attenuated, so it will be important to consider this factor in future studies. Nonetheless, our results indicate that winter warming could negatively impact cold‐adapted insects such as the Antarctic midge. Read the free Plain Language Summary for this article on the Journal blog.

Chironomid midges (Diptera) provide insights into genome evolution in extreme environments.

Extremophiles often undergo marked changes in genomic architecture, likely as a result of adaptation to the harsh environments they inhabit. These changes can involve gene duplications that affect subsequent gene evolution and the regulation of gene expression. Excellent examples of this are provided by two non-biting chironomid midges (Diptera, Chironomidae): Polypedilum vanderplanki, which in its larval form can withstand almost complete water loss, and Belgica antarctica, which exhibits freeze tolerance. This review presents recent studies on the molecular adaptations and evolutionary features of these and other extremophile chironomid genomes, as well as biotechnological applications of a cell line derived from P. vanderplanki that can survive air-drying. We highlight the importance of genomics in identifying molecular pathways and genomic modifications associated with adaptation to extreme environmental conditions.

Fine-scale variation in microhabitat conditions influences physiology and metabolism in an Antarctic insect.

Microhabitats with distinct biotic and abiotic properties exist within landscapes, and this microhabitat variation can have dramatic impacts on the phenology and physiology of the organisms occupying them. The Antarctic midge Belgica antarctica inhabits diverse microhabitats along the Western Antarctic Peninsula that vary in macrophyte composition, hygric qualities, nutrient input, and thermal patterns. Here, we compare seasonal physiological changes in five populations of B. antarctica living in close proximity but in different microhabitats in the vicinity of Palmer Station, Antarctica. Thermal regimes among our sample locations differed in both mean temperature and thermal stability. Between the warmest and coldest sites, seasonal mean temperatures differed by 2.6˚C and degree day accumulations above freezing differed by a factor of 1.7. Larval metabolic and growth rates varied among the sites, and adult emergence occurred at different times. Distinct microhabitats also corresponded with differences in body composition, as lipid and carbohydrate content of larvae differed across sites. Further, seasonal changes in carbohydrate and protein content were dependent on site, indicating fine-scale variation in the biochemical composition of larvae as they prepare for winter. Together, these results demonstrate that variation in microhabitat properties influences the ontogeny, phenology, physiology, and biochemical makeup of midge populations living in close proximity. These results have implications for predicting responses of Antarctic ecosystems to environmental change.

External Morphology of Larvae of Belgica antarctica Jacobs, 1900 (Diptera, Chironomidae) Obtained from Two Locations in Maritime Antarctica.

Simple SummaryThe chironomid midge Belgica antarctica Jacobs is endemic to the western Antarctic Peninsula and South Shetland Islands. We provide the first detailed photomicrographic images of the fourth-instar larval head capsule and posterior parapods. We assessed variation in the morphology of larvae from two different collection locations off the coast of the western Antarctic Peninsula and compared it with that available in the literature. A number of differences were identified relating to the size of the larvae, the number of teeth on the mandibles, the number of antennal segments and the length of the antennal blade. Malformations of the mandible and mentum are reported for the first time in this species.The external morphology of the fourth-instar larva of the Antarctic endemic chironomid midge Belgica antarctica is described. Larvae were collected from Jougla Point (Wiencke Island) and an un-named island close to Enterprise Island, off the coast of the western Antarctic Peninsula. Light microscopy was used to examine and document photographically the structures of the mouthparts (mandible, mentum, premandible, labrum), antennae, pecten epipharyngis, clypeus, frontal apotome and posterior parapods. Measurements of the mouthparts are presented. The data obtained are compared with that available in the literature. A number of differences were identified relating to the size of the larvae, the number of teeth on the mandibles, the number of antennal segments and the length of the antennal blade. Malformations of the mandible and mentum are reported for the first time in this species. Features of larvae of taxonomic value that can be used to determine the species in larval stages are presented. These are of utility in using the larvae to reveal relationships with other species. Larvae are also important in ecological and genotoxicological studies, which require accurate species level identification.

Long-term retainment of some chromosomal inversions in a local population of Belgica antarctica Jacobs (Diptera, Chironomidae)

Genome of antarctic endemic Belgica antarctica Jacobs has been sequenced. However, no set of inversion diagnostic markers has ever been assigned for the species. Using the classical method of polytene chromosome squash preparation, we found three heterozygous inversions located on the second (two heterozygous inversions) and third chromosomes (one heterozygous inversion) in the Belgica antarctica population of a cape of Wiencke Island, 500 m to SW from Port Lockroy. The chromosome set and chromosome variability did not differ from those described in the literature (Atchley and Davis 1979). Every salivary gland chromosome had its own markers by which it can be determined. However, we did not find a sex-linked inversion on chromosome III and heterozygous inversion on chromosome I, reported in earlier studies. For the first time, we observed a strong heterochromatin band in chromosome III at the telomere of one arm. Our data show not only the stability of the described inversions in the population but also the usefulness of the squash preparation technique in the studies of genetic variability of Belgica antarctica in present time.

Rapid stress hardening in the Antarctic midge improves male fertility by increasing courtship success and preventing decline of accessory gland proteins following cold exposure.

Rapid hardening is a process that quickly improves an animal's performance following exposure to potentially damaging stress. In this study of the Antarctic midge, Belgica antarctica (Diptera, Chironomidae), we examined how rapid hardening in response to dehydration (RDH) or cold (RCH) improves male pre- and post-copulatory function when the insects are subsequently subjected to a damaging cold exposure. Neither RDH nor RCH improved survival in response to lethal cold stress, but male activity and mating success following sublethal cold exposure were enhanced. Egg viability decreased following direct exposure of the mating males to sublethal cold but improved following RCH and RDH. Sublethal cold exposure reduced the expression of four accessory gland proteins, while expression remained high in males exposed to RCH. Though rapid hardening may be cryptic in males, this study shows that it can be revealed by pre- and post-copulatory interactions with females.

Belgica antarctica (Diptera: Chironomidae): A natural model organism for extreme environments.

Belgica antarctica (Diptera: Chironomidae), a brachypterous midge endemic to the maritime Antarctic, was first described in 1900. Over more than a century of study, a vast amount of information has been compiled on the species (3 750 000 Google search results as of January 10,2021), encompassing its ecology and biology, life cycle and reproduction, polytene chromosomes, physiology, biochemistry and, increasingly, omics. In 2014, B. antarctica's genome was sequenced, further boosting research. Certain developmental stages can be cultured successfully in the laboratory. Taken together, this wealth of information allows the species to be viewed as a natural model organism for studies of adaptation and function in extreme environments.

Expression of aquaporins in response to distinct dehydration stresses that confer stress tolerance in the Antarctic midge Belgica antarctica

Larvae of the Antarctic midge Belgica antarctica Jacobs (Diptera: Chironomidae) are highly tolerant of diverse environmental stresses, including freezing, severe desiccation, and osmotic extremes. Furthermore, dehydration confers subsequent desiccation and freeze tolerance. While a role for aquaporins—channels for water and other solutes—has been proposed in these dehydration processes, the types of aquaporins involved in dehydration-driven stress tolerance remain unknown. In the present study, we investigated expression of six aquaporins (Drip, Prip, Eglp1, Eglp2, Aqp12L, and Bib) in larvae of B. antarctica subjected to three different dehydration conditions: desiccation, cryoprotective dehydration, and osmotic dehydration. The expression of Drip and Prip was up-regulated under desiccation and cryoprotective dehydration, suggesting a role for these aquaporins in efficient water loss under these dehydration conditions. Conversely, expression of Drip and Prip was down-regulated under osmotic dehydration, suggesting that their expression is suppressed in larvae to combat dehydration. Larval water content was similarly decreased under all three dehydration conditions. Differences in responses of the aquaporins to the three forms of dehydration suggests distinct water management strategies associated with different forms of dehydration stress.

Current status of Belgica antarctica Jacobs, 1900 (Diptera: Chironomidae) distribution by the data of Ukrainian Antarctic Expeditions

Given the recent climate changes and their impact on the Antarctic Peninsula ecosystems, the emergence of invasive species, and increased tourism activity in this region, monitoring changes in the habitats of species native to the Antarctic Peninsula region is necessary. One such species is the Antarctic midge Belgica antarctica (Chironomidae). This insect is endemic to the Antarctic Peninsula and adjacent islands. Thorough studies of changes in the range of this species have not been performed in recent decades. In this study, we present the area of Belgica antarctica according to the collections of biological samples during 2007–2021 (XII, XIV, XVI, XXIV, and XXV Ukrainian Antarctic Expeditions). This Antarctic midge was recorded at 26 localities on the Antarctic Peninsula and 212 localities on 55 surrounding islands between 66°08′38.4′′ S, 65°43′37.1′′ W (Cape Evensen, Stresher Peninsula, opposite the Marie Island, west coast of Graham Land) and 62°11′44.7′′ S, 58°57′40.6′′ W (King George Island, South Shetland Islands) from south-west to north-east.

Multi-level analysis of reproduction in an Antarctic midge identifies female and male accessory gland products that are altered by larval stress and impact progeny viability

The Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least 2 years, but adults live only 2 weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology. RNA-seq analyses revealed sex- and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source as well as a buffer for thermal and dehydration stress. All of these function are critical to juvenile survival. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may have a significant impact on population growth. This work lays a foundation for further examination of reproduction in midges and provides new information related to general reproduction in dipterans. A key aspect of this work is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical in determining how climate change will alter their survivability.

Environmental factors influencing fine-scale distribution of Antarctica\u2019s only endemic insect

Species distributions are dependent on interactions with abiotic and biotic factors in the environment. Abiotic factors like temperature, moisture, and soil nutrients, along with biotic interactions within and between species, can all have strong influences on spatial distributions of plants and animals. Terrestrial Antarctic habitats are relatively simple and thus good systems to study ecological factors that drive species distributions and abundance. However, these environments are also sensitive to perturbation, and thus understanding the ecological drivers of species distribution is critical for predicting responses to environmental change. The Antarctic midge, Belgica antarctica, is the only endemic insect on the continent and has a patchy distribution along the Antarctic Peninsula. While its life history and physiology are well studied, factors that underlie variation in population density within its range are unknown. Previous work on Antarctic microfauna indicates that distribution over broad scales is primarily regulated by soil moisture, nitrogen content, and the presence of suitable plant life, but whether these patterns are true over smaller spatial scales has not been investigated. Here we sampled midges across five islands on the Antarctic Peninsula and tested a series of hypotheses to determine the relative influences of abiotic and biotic factors on midge abundance. While historical literature suggests that Antarctic organisms are limited by the abiotic environment, our best-supported hypothesis indicated that abundance is predicted by a combination of abiotic and biotic conditions. Our results are consistent with a growing body of literature that biotic interactions are more important in Antarctic ecosystems than historically appreciated.

Assessing distribution shifts and ecophysiological characteristics of the only Antarctic winged midge under climate change scenarios

Parts of Antarctica were amongst the most rapidly changing regions of the planet during the second half of the Twentieth Century. Even so, today, most of Antarctica remains in the grip of continental ice sheets, with only about 0.2% of its overall area being ice-free. The continent’s terrestrial fauna consists only of invertebrates, with just two native species of insects, the chironomid midges Parochlus steinenii and Belgica antarctica. We integrate ecophysiological information with the development of new high-resolution climatic layers for Antarctica, to better understand how the distribution of P. steinenii may respond to change over the next century under different IPCC climate change scenarios. We conclude that the species has the potential to expand its distribution to include parts of the west and east coasts of the Antarctic Peninsula and even coastal ice-free areas in parts of continental Antarctica. We propose P. steinenii as an effective native sentinel and indicator species of climate change in the Antarctic.

RNA secondary structures in Dscam1 mutually exclusive splicing: unique evolutionary signature from the midge.

The Drosophila melanogaster gene Dscam1 potentially generates 38,016 distinct isoforms via mutually exclusive splicing, which are required for both nervous and immune functions. However, the mechanism underlying splicing regulation remains obscure. Here we show apparent evolutionary signatures characteristic of competing RNA secondary structures in exon clusters 6 and 9 of Dscam1 in the two midge species (Belgica antarctica and Clunio marinus). Surprisingly, midge Dscam1 encodes only ∼6000 different isoforms through mutually exclusive splicing. Strikingly, the docking site of the exon 6 cluster is conserved in almost all insects and crustaceans but is specific in the midge; however, the docking site-selector base-pairings are conserved. Moreover, the docking site is complementary to all predicted selector sequences downstream from every variable exon 9 of the midge Dscam1, which is in accordance with the broad spectrum of their isoform expression. This suggests that these cis-elements mainly function through the formation of long-range base-pairings. This study provides a vital insight into the evolution and mechanism of Dscam1 alternative splicing.

Changes in Energy Reserves and Gene Expression Elicited by Freezing and Supercooling in the Antarctic Midge, Belgica antarctica.

Freeze-tolerance, or the ability to survive internal ice formation, is relatively rare among insects. Larvae of the Antarctic midge Belgica antarctica are freeze-tolerant year-round, but in dry environments, the larvae can remain supercooled (i.e., unfrozen) at subzero temperatures. In previous work with summer-acclimatized larvae, we showed that freezing is considerably more stressful than remaining supercooled. Here, these findings are extended by comparing survival, tissue damage, energetic costs, and stress gene expression in larvae that have undergone an artificial winter acclimation regime and are either frozen or supercooled at −5 °C. In contrast to summer larvae, winter larvae survive at −5 °C equally well for up to 14 days, whether frozen or supercooled, and there is no tissue damage at these conditions. In subsequent experiments, we measured energy stores and stress gene expression following cold exposure at −5 °C for either 24 h or 14 days, with and without a 12 h recovery period. We observed slight energetic costs to freezing, as frozen larvae tended to have lower glycogen stores across all groups. In addition, the abundance of two heat shock protein transcripts, hsp60 and hsp90, tended to be higher in frozen larvae, indicating higher levels of protein damage following freezing. Together, these results indicate a slight cost to being frozen relative to remaining supercooled, which may have implications for the selection of hibernacula and responses to climate change.

Onset of seasonal metabolic depression in the Antarctic midge Belgica antarctica appears to be independent of environmental cues

AbstractSeasonal progression is tracked in most animals by changes in daylength, thus allowing reliable synchrony with abundant food and favourable developmental conditions. In polar regions, daylength varies extensively, fluctuating at the highest latitudes from persistent light to persistent dark. The Antarctic midge Belgica antarctica has a narrow seasonal window in which to feed and develop, and previous work shows that this insect, despite having the elements of a circadian clock, remains continuously active when temperatures are permissive. The present study aims to clarify seasonal tracking in B. antarctica during the austral summer by monitoring oxygen consumption rates in a field population and in experimental groups exposed to shortened daylength, dehydration and chilling. Remarkably, during March, coordinated decreases in oxygen consumption are observed, ranging from 18% to 42%, in all treatment groups, indicating an anticipatory response to seasonal change regardless of the environmental cues. These results suggest that B. antarctica relies on an intrinsic mechanism to program metabolic depression at the onset of the long austral winter.

Characterization of drought-induced rapid cold-hardening in the Antarctic midge, Belgica antarctica

Survival of the terrestrial midge, Belgica antarctica, on the Antarctic Peninsula is promoted, not only by their adaptations to prolonged exposures to seasonal stresses, but also by their ability to respond to unpredictable changes in their environments. Rapid cold-hardening (RCH) is an extremely swift acclimatory response of insects that occurs within minutes to hours. While the RCH response is most commonly induced by a brief exposure to mildly low temperatures, a similar rapid acclimatory response can also be elicited by exposure to drought. In this study, we characterized this drought-induced RCH in larvae of B. antarctica. Compared to fully hydrated larvae, those desiccated at various relative humidity (R.H.) conditions between 0 and 99% R.H. for 2 h had a significantly greater survival ( ~ 50%) to freezing at − 14 °C. The amount of water loss varied between 4 and 16% depending on R.H. conditions; however, all treatments were equally effective in eliciting the protective response against freezing stress, and its induction was evident within 30 min of desiccation. Lack of substantial changes in body-fluid osmolality or levels of major cryoprotectants suggest that accumulation of these protective solutes is not a primary mechanism of this response. Interestingly, the RCH protection induced by desiccation persisted after larvae were allowed to recover a significant portion of the lost water. Our results indicate that larval midges are highly sensitive to desiccation, capable of swiftly initiating physiological changes in response to a small reduction in their body water content.