An international research team shows that a newly discovered nematode <span class="glossaryLink" aria-describedby="tt" data-cmtooltip="
” data-gt-translate-attributes=”["attribute":"data-cmtooltip", "format":"html"]”>species from the Pleistocene share a molecular toolkit for survival with the nematode Caenorhabditis elegans.
Some organisms, such as tardigrades, rotifers, and nematodes, can survive harsh conditions by entering a dormant state known as “cryptobiosis.” In 2018, researchers from the Institute of Physicochemical and Biological Problems in Soil Science RAS in Russia found two roundworms (nematode) species in the Siberian Permafrost. Radiocarbon dating indicated that the nematode individuals have remained in cryptobiosis since the late Pleistocene, about 46,000 years ago.
Researchers from the Max Planck Institute of <span class="glossaryLink" aria-describedby="tt" data-cmtooltip="
” data-gt-translate-attributes=”["attribute":"data-cmtooltip", "format":"html"]”>Molecular Cell Biology and Genetics (MPI-CBG) in Dresden, the Center for Systems Biology Dresden (CSBD), and the Institute of Zoology at the University of Cologne, all located in Germany, used genome sequencing, assembly, and phylogenetic analysis and found that the permafrost nematode belongs to a previously undescribed species, Panagrolaimus kolymaensis. They showed that the biochemical mechanisms employed by Panagrolaimus kolymaensis to survive desiccation and freezing under laboratory conditions are similar to those of a life-cycle stage in the important biological model Caenorhabditis elegant.
Revival and Initial Investigation of the Nematodes
When Anastasia Shatilovich at the Institute of Physicochemical and Biological Problems in Soil Science RAS in Russia revived two frozen individual nematodes from a fossilized burrow in silt deposits in the Siberian permafrost, she and her colleagues were beyond excited. After thawing the worms in the lab, a radiocarbon analysis of plant material from the burrow revealed that these frozen deposits, 40 meters below the surface, had not thawed since the late Pleistocene, between 45,839 and 47,769 years ago.
At the same time, the research group of Teymuras Kurzchalia at the MPI-CBG (Teymuras Kurzchalia is now retired) was already addressing the question of how larval stages of the nematode Caenorhabditis elegans survive extreme conditions. When the team heard about the permafrost nematodes, they immediately reached out for a collaboration with Anastasia Shatilovich.
Collaboration and Further Research
Vamshidhar Gade, a doctoral student at that time in the research group of Teymuras Kurzchalia, started to work with the permafrost nematodes. “What molecular and metabolic pathways these cryptobiotic organisms use and how long they would be able to suspend life are not fully understood,” he says. Vamshidhar is now working at the ETH in Zurich, Switzerland.
Genome Analysis and Species Identification
The researchers in Dresden conducted a high-quality genome assembly of one of the permafrost nematodes in collaboration with Eugene Myers, Director Emeritus and research group leader at the MPI-CBG, the DRESDEN-concept Genome Center, and the research group of Michael Hiller, research group leader at that time at the MPI-CBG and now Professor of Comparative Genomics at the LOEWE-TBG and the Senckenberg Society for Nature Research. Despite having <span class="glossaryLink" aria-describedby="tt" data-cmtooltip="
” data-gt-translate-attributes=”["attribute":"data-cmtooltip", "format":"html"]”>DNA barcoding sequences and microscopic pictures, it was difficult to determine whether the permafrost worm was a new species or not.
Philipp Schiffer, research group leader at the Institute of Zoology, co-lead of the incipient Biodiversity Genomics Center Cologne (BioC2) at the University of Cologne, and expert in biodiversity genomics research, joined forces with the Dresden researchers to determine the species and analyze its genome with his team. Using phylogenomic analysis, he and his team were able to define the roundworm as a novel species, and the team decided to call it “Panagrolaimus kolymaensis.” In recognition of the Kolyma River region from which it originated, the nematode was given the Latin name Kolymaensis.
Survival Mechanism and Potential Implications
By comparing the genome of Panagrolaimus kolymaensis with that of the model nematode Caenorhabditis elegans, the researchers in Cologne identified genes that both species have in common and that are involved in cryptobiosis. To their surprise, most of the genes necessary for entering cryptobiosis in Caenorhabditis elegans so-called Dauer larvae were also present in Panagrolaimus kolymaensis.
Next, the research team evaluated Panagrolaimus kolymaensis’s ability to survive and discovered that mild dehydration exposure before freezing helped the worms prepare for cryptobiosis and increased survival at -80 degrees <span class="glossaryLink" aria-describedby="tt" data-cmtooltip="
” data-gt-translate-attributes=”["attribute":"data-cmtooltip", "format":"html"]”>Celsius. At a biochemical level, both species produced a sugar called trehalose when mildly dehydrated in the lab, possibly enabling them to endure freezing and intense dehydration. Caenorhabditis elegans larvae also benefited from this treatment, surviving for 480 days at -80 degrees Celsius without suffering any declines in viability or reproduction following thawing.
According to Vamshidhar Gade and Temo Kurzhchalia, “Our experimental findings also show that Caenorhabditis elegans can remain viable for longer periods in a suspended state than previously documented. Overall, our research demonstrates that nematodes have developed mechanisms that allow them to preserve life for geological time periods.”
“Our findings are essential for understanding evolutionary processes because generation times can range from days to millennia and because the long-term survival of a species’ individuals can result in the re-emergence of lineages that would otherwise have gone extinct,” concludes Philipp Schiffer, one of the authors who oversaw the study.
Eugene Myers adds: “P. kolymaensis‘s highly contiguous genome will make it possible to compare this feature to those of other Panagrolaimus species whose genomes are presently being sequenced by Schiffer’s team and colleagues.” Philipp Schiffer is convinced that “studying the adaptation of species to such extreme environments by analyzing their genomes will allow us to develop better conservation strategies in the face of global warming.”
Teymuras Kurzchalia says: “This study extends the longest reported cryptobiosis in nematodes by tens of thousands of years.”
Reference: “A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva” by Anastasia Shatilovich, Vamshidhar R. Gade, Martin Pippel, Tarja T. Hoffmeyer, Alexei V. Tchesunov, Lewis Stevens, Sylke Winkler, Graham M. Hughes, Sofia Traikov, Michael Hiller, Elizaveta Rivkina, Philipp H. Schiffer, Eugene W. Myers and Teymuras V. Kurzchalia, 27 July 2023, PLoS Genetics.
This work was supported by the Russian Foundation fr Basic Research (19-29-05003-mk) to AS and ER. VRG and TVK acknowledge the financial support from the Volkswagen Foundation (Life research grant 92847). PHS and TTH are supported by a DFG ENP grant to PHS (DFG project 434028868). GMH is funded by a UCD Ad Astra Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Sea ice around Antarctica recedes to historically low levels: Scientists
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Soyuz docks at International Space Station with two Russians, one American
A Russian spacecraft carrying two Russians and an American docked at the International Space Station on Friday after blasting off from Kazakhstan.
NASA astronaut Loral O’Hara and Roscosmos cosmonauts Oleg Kononenko and Nikolai Chub departed from the Baikonur Cosmodrome in Kazakhstan and docked at the ISS approximately three hours later.
Per NASA, the trio will join the station’s Expedition 69 crew comprising astronauts from the U.S., Russia, Denmark, and Japan. O’Hara will spend six months there while Kononenko and Chub will spend a year.
The trio was supposed to fly to the space station earlier this year, but their original capsule, Soyuz MS-23, was needed as a replacement for another crew. That crew — also two Russians and an American — will ride it home on September 27. Their stay was extended from six months to a year when the capsule developed a coolant leak while parked at the station.
It’s the first spaceflight for O’Hara and Chub, while mission commander Kononenko is on his fifth trip to the orbiting outpost. By the end of his yearlong stay, Kononenko will set a new record for the longest time in space, more than a thousand days.
Original article source: Soyuz docks at International Space Station with two Russians, one American
Exploring the effect of pain on response to reward loss in calves
Negative emotional states are known to interact, potentially aggravating one another. In this study, we used a well validated paradigm (successive negative contrast, SNC) to determine if pain from a common procedure (disbudding) influences responses to a reward downshift. Holstein calves (n = 30) were trained to approach a 0.5 L milk reward. Latency to approach, number of vocalisations and pressure applied on the bottle were recorded during training. To assess how pain affected responses to reward downshift, calves were randomly assigned to one of three treatments before the downshift. Two groups were disbudded and provided the ‘gold standard’ of pain mitigation: intraoperative local anesthesia and analgesia. One of these disbudded groups was then provided supplemental analgesic before testing. The third group was sham disbudded. All calves were then subjected to the reward downshift by reducing the milk reward to just 0.1 L. Interactions were detected between test session and daily trials on pressure applied for the Disbudded group (estimate ± SEM: 0.08 ± 0.05), and on vocalisations for the Sham (0.3 ± 0.1) and Disbudding + Analgesia (0.4 ± 0.1) groups. Our results indicate that SNC is a promising paradigm for measuring negative affect in calves and suggests that pain potentially affects the response to a reward downshift.
A large body of research, primarily on rodents, has shown that sudden declines in reward levels are highly salient and provoke a negative affective response consistent with feelings of frustration or disappointment1,2. A well-developed paradigm for provoking this response is the successive negative contrast (SNC) test, where animals learn to obtain feed rewards which are then reduced in quantity or quality. Multiple lines of evidence indicate that this experience is distressing for animals, including increased levels of physiological markers of stress in rats and pigs3,4,5, and development of a preference for anxiolytic medication in rats6. In addition, responses to SNC are aggravated when an animal is in a pre-existing negative emotional state at the time of the test. For example, rats bred to be more anxious had higher latencies to approach a reward after a downshift7, and rats in amphetamine withdrawal displayed greater and longer reductions in reward consumption following a downshift8.
The influence of current affective state on SNC responses provides a compelling opportunity for the assessment of animal welfare, although only a handful of studies have employed this approach. In one study, rats housed in barren environments showed an extended increase in latency to approach the downshifted reward in comparison to rats housed in enriched environments, suggesting that these animals were more sensitive to reward loss than were rats in enriched housing9. Housing conditions (barren vs. enriched) also affected pigs’ sensitivity to reward loss10. To our knowledge, SNC has not been used to assess the emotional impact of pain in any species.
In this study we tested if pain aggravates responses to SNC testing. Young cattle experience pain associated with routine farm procedures including hot-iron disbudding, indicated by physiological, behavioral and emotional responses to the procedure14,15,16,17,18. In this study we assessed the responses to SNC (in this case reducing the amount of milk available) in calves for three days following disbudding. Although providing a combination of local anesthesia and analgesia is considered a gold-standard in pain mitigation following disbudding, the duration of pain control has been challenging to estimate18, and disbudding pain has been suggested to last for several days19,20,21. For ethical reasons, all disbudded calves were provided local anesthesia and analgesia at the time of the procedure. To explore the potential longer-term pain caused by disbudding, a group of calves were provided additional fast-acting analgesia before tests. We predicted that calves in pain would respond to the downshift by increased pressure applied on the bottle containing the milk, number of vocalisations and latency to approach the reward. By exploring a novel approach to assessing the affective component of pain in animals, we hope to further the understanding of the emotional impact of a common farm procedure and, more generally, how negative states can interact to influence animal welfare.
Maximum pressure applied to the reward bottle decreased across test days (− 0.4, t = − 3.5, P = 0.005) and daily trials (− 0.3, t = − 2.6, P = 0.01) (Fig. 1A). We also noted an interaction between test day and daily trial for the Disbudded group (0.1, t = 2.0, P = 0.05), and a tendency for the Sham group (0.08, t = 1.7, P = 0.09). There was no evidence of an interaction for pressure in the Disbudding + Analgesia group (0.07, t = 1.4, P = 0.2). Calves produced fewer vocalisations across days (− 1.5, t = − 4.6, P < 0.001) and daily trials (− 0.8, t = − 3.6, P < 0.001) (Fig. 1B). However, there were positive interactions between test day and trials for the Sham and Disbudding + Analgesia groups (0.3, t = 2.0, P = 0.05; 0.4, t = 2.7, P < 0.001 respectively). No interaction was found for the Disbudding group (0.05, t = 0.3, P = 0.7). Calves took longer to approach the reward across daily trials (0.4, t = 3.1, P = 0.002), with no effect of the test day (0.12, t = 0.9, P = 0.4) (Fig. 1C). Calves from the Sham group tended to decrease their latency across test day and daily trial (− 0.11, t = − 1.7, P = 0.09), whereas no interaction was found for the Disbudding (− 0.02, t = − 0.3, P = 0.8) and Disbudding + Analgesia groups (− 0.06, t = − 0.9, P = 0.3).
After the reward downshift, calves responded by high pressure applied to the bottle and vocalisations. As calves went through more test sessions (with the lower reward), vocalisations and pressure both decreased, suggesting calves updated their expectations over time. Following the downshift, calves also increased their approach latency across trials within daily test sessions. This result is consistent with previous reports noting that approach latency increased after reward downshift 9,22.
We found some indication of a treatment effect on responses to the downshift over test days and daily trials. The significant positive interaction in pressure applied on the bottle over days and trials for the Disbudding group suggests some level of maintained frustration over tests. Similarly, only calves who had not been disbudded tended to decrease their approach latency across trials whereas calves from the Disbudding and Disbudding + Analgesia groups maintained their latency increase. This result is consistent with results from Burman and colleagues9 who reported a more prolonged response to reward downshift (i.e. higher latency) from rats assumed to be in a more negative affective state. This result is also consistent with work on calves showing increased anticipatory behavior in response to a reward downshift for animals housed in a more barren environment23. We had expected that calves receiving supplemental ketoprofen before the daily test sessions would have responded similarly to the sham calves. That these animals appeared to have some similar responses to the other disbudded calves suggests that our ketoprofen treatment protocol might not have mitigated the pain associated with disbudding during tests. Ketoprofen has been noted as appropriate pain control for disbudding24,25,26,27, but conflicting results have also been reported28,29.
In a study on SNC in chickens, Davies and colleagues30 found a gradual increase in approach latency and an immediate response in consummatory behaviours. They noted the gradual increase to be consistent with Thorndike’s law of effect31, analogous to an extinction mechanism where a less valuable reward induces a less ‘enthusiastic’ response over time. The disparity with consummatory responses was suggested to relate to the different timeframes of the measures: anticipatory responses such as approach latency might require conditioned learning, and therefore change more slowly. However, consummatory responses such as pressure applied are immediate indicators of reward evaluation, and therefore do not require an adjustment delay.
Contrary to our predictions, calves from the Disbudding group did not vocalize more than the other treatment groups after the downshift. These results remain unclear to us, but the very low number of vocalisations past the first test day questions the sensitivity of calves vocalisations counts when used in SNC paradigms.
The high variability among calves in their response to the downshift could be associated to intrinsic individual differences. Individual differences in traits such as fearfulness have been linked to pessimistic responses to a judgment bias test32. Moreover, such pessimism was also linked to the anhedonic response (i.e. a decrease in interest in a consummatory reward) following hot-iron disbudding33. Calves’ individual differences could also be dependent on the severity of the sensitization of their head caused by the procedure34,35, causing increased pain when coming into contact with the bottle. Alternatively, sucking on the nipple (even without milk) may be positive for calves36 and may also provide pain relief in the hours after disbudding37.
Following a reduction in a milk reward, calves who experienced a painful procedure appeared to potentially display an extended response to the downshift. Although SNC seems a promising avenue, our results remain tentative and further development of the paradigm and its applications must be investigated to identify its relevance to animal welfare assessment.
Procedures were approved by The University of British Columbia Animal Care Committee under application A21-0111 and conducted in accordance with guidelines form the Canadian Council of Animal Care38. Reporting followed ARRIVE guidelines.
Animals and housing
The study was conducted at The University of British Columbia’s Dairy Education and Research Centre. To our knowledge, no study has used a similar paradigm in calves. To establish a sample size estimate, we relied on welfare studies using analogous SNC paradigms but applied to other species: rats (six subject per treatment9) and pigs (sixteen subjects per treatment group10). Considering this range and our own practical limitations, we settled on a sample size of ten subjects per treatment group. Thirty-five Holstein calves (all females) were initially enrolled in the study. Five calves were removed from the trial: three fell ill (scours and fever), one showed an extreme stress response when moved outside of her home pen, and one was not feed-restricted before a test. The thirty remaining had an average (± SD) birth weight of 38.3 ± 4.1 kg and were enrolled at 39.9 ± 4.1 d of age.
As routine farm practice, calves from all three treatments were intermingled in indoor pens (4.9 × 7.3 m, bedded with sawdust, and each containing eight to ten calves). Calves were provided ad libitum access to water and hay (RIC; Insentec B.V., Netherlands), and time-restricted access to 12 L of whole milk through a nipple feeder (CF 1000 CS Combi; DeLaval Inc., Sweden). To avoid long delay during trials, small replicates (average number of subjects per replicate = 3.5) were conducted.
The experimental apparatus was located in the same barn as the calves’ home pen, approximately 10–30 m away. The apparatus was a 1.8 × 1.2 m start-box leading to a 3.6 × 2.4 m pen through a vertical gate (Fig. 2A). Directly across from the start-box was a bottle and rubber teat mounted on rails, with an algometer (FPX 25, Wagner, Greenwich, USA) installed behind the bottle allowing measures of the maximum pressure applied to the bottle (Fig. 2B).
The trial was divided in three phases over seven days: training (three days), treatment (one day) and testing (three days). During training, calves were feed-restricted overnight (from 22:00 h) to ensure a high motivation for milk rewards over repeated trials. At approximately 10:00 h calves were individually brought into the apparatus, with no set order, and then placed in the start-box. The vertical gate was lifted and calves could approach and drink a 0.5 L milk reward from the bottle (this amount was based on previous studies on motivation trade-offs studies in calves37,39). Latency to contact the bottle (with mouth or tongue), latency to finish the reward, number of vocalisations and maximum pressure applied to the bottle were recorded live. The calf was then brought back to the start-box, the bottle refilled, and two more trials were conducted (i.e., for a total of three trials/d). After these trials were completed, the calf was returned to her home pen with full access to her daily milk allowance of (12 L/d). Training took place over three consecutive days, for a total of nine training trials. During the first day of training (for all three trials), no cues were given to the calf for the first minute after opening the start-box gate. After one minute, auditory (calls/whistle) and tactile (finger suckling) cues were given from the experimenter from outside the test-pen to get the calf’s attention towards the bottle. If these cues had failed after an additional minute, the experimenter would go inside the test pen and lead the calf to the bottle.
During the second and third day of training, no cues were given. If the calf had not approached the bottle within two minutes, the trial was recorded as a no-approach (and a pressure of zero applied to the bottle). Once a calf had approached the bottle, she had three additional minutes to finish the reward.
Calves were pseudo-randomly assigned to one of three treatments (Disbudding, Disbudding + Analgesia, or Sham; ten calves each). Treatment assignment was balanced for age and birthweight (Disbudding: 40.7 ± 4.3 d, 38.7 ± 3.9 kg; Disbudding + Analgesia: 39.2 ± 7.0 d, 38.0 ± 5.6 kg; Sham: 39.7 ± 6.0 d, 38.3 ± 2.4 kg). On treatment day, calves were not feed-restricted and went through their treatment in their group pen at approximately 10:00 h. Regardless of treatment, calves were weighted and administered a multimodal pain mitigation strategy of sedative, local anesthesia and analgesia. The sedative was used to facilitate following injections and disbudding (xylazine 0.2 mg/kg Subcutaneous, Rompun 20 mg/mL, Bayer, Leverkusen, Germany). After sedation was reached (recumbency and eye rotation, approximately 10 min), a local anesthetic was injected as a cornual nerve block to mitigate the acute pain of the procedure (5 mL per side, lidocaine 2%, epinephrine 1:100,000, Lido-2, Rafter8, Calgary, AB, Canada), an NSAID was provided to minimize inflammation (meloxicam 0.5 mg/kg Subcutaneous, Metacam 20 mg/mL, Boehringer Ingelheim, Burlington, ON, Canada), and the horn bud area was shaved with an electric trimmer. Ten minutes after lidocaine injection, a pinprick test was done on the horn buds to test for pain reflex. For calves in the Disbudding and Disbudding + Analgesia treatments, a pre-heated electric dehorner (X30, 1.3 cm tip, Rhinehart, Spencerville, IN, USA) was applied to both horn buds until a consistent dark ring formed around each bud (requiring approximately 10 to 15 s). Calves from the Sham group were treated identically but instead of being disbudded, only pressure on the horn buds was applied with the plastic handle of the dehorner. After the procedure was completed, calves were positioned in sternal recumbency and left to recover in the pen. As the magnitude and duration of NSAID effects following disbudding remain unclear 18, calves from the Disbudding + Analgesia group received an additional NSAID injection (ketoprofen, 3 mg/kg, Subcutaneous, Anafen, 100 mg/mL, Boehringer Ingelheim, Ontario, Canada) 1 h before each of the three test sessions to provide supplemental pain control at the time of testing. Based on a previous study on the efficacy of ketoprofen after disbudding29, we expected ketoprofen to provide analgesic effects for up to 2 h following treatment.
In the three days following treatment, calves were tested for sensitivity to reward loss. Tests were similar to training: calves were brought individually to the apparatus after overnight feed restriction, and allowed access to a milk reward three times in a row (for a total of nine trials), but during testing the reward was reduced to 0.1 L. The time allowed for calves to approach and drink the reward was matched with their performance during training. Maximum pressure applied to the bottle, number of vocalisations and latency to approach were recorded. Calves from the Disbudding + Analgesia group received an additional NSAID injection (ketoprofen, 3 mg/kg, Subcutaneous, Anafen, 100 mg/mL, Boehringer Ingelheim, Ontario, Canada) 1 h before each of the three test sessions. After each session calves were returned to their home pen and again provided access to their full milk allowance (12 L). After the three test days calves were returned to routine farm care.
A mixed model was conducted on each outcome (maximum pressure, vocalisations and approach latency) on test phases (post treatment) using R’s lme4 package40. For pressure and latency, data were log transformed to fit model assumptions of linearity, normality and homoscedasticity. For vocalisation counts, we used a Poisson mixed model. Fixed factors were treatment (2 df), test day (1 df), daily trial (1 df) and their interaction (3 df). Daily trial, nested within day and Calf ID, was included as a random factor. Significance and tendency thresholds were set at P ≤ 0.05 and P ≤ 0.10, respectively. Data (Supplementary Information 1) and R code (Supplementary Information 2) are available in supplementary materials.
The dataset and R code are freely available in supplementary materials.
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We thank the staff and students at The UBC Dairy Education and Research Centre for their help and support. We are especially grateful for the help provided by (alphabetical order) Joseph Lee, Kathen Lee, Emeline Nogues, Zimbabwe Osorio, Yasamin (Yas) Ranjbar, Russell Tucker, Raphaela Woodroffe and Emily Yau. This research was funded by a Discovery Grant (RGPIN-2016-0462) awarded to DMW from the National Sciences and Engineering Research Council of Canada.
The authors declare no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Cite this article
Ede, T., von Keyserlingk, M.A.G. & Weary, D.M. Exploring the effect of pain on response to reward loss in calves.
Sci Rep 13, 15403 (2023). https://doi.org/10.1038/s41598-023-42740-8
- Received: 05 December 2022
- Accepted: 14 September 2023
- Published: 16 September 2023
- DOI: https://doi.org/10.1038/s41598-023-42740-8
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