Latitudinal differences in the circadian system of Nasonia vitripennis Floessner, Theresa
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Floessner, T. (2019). Latitudinal differences in the circadian system of Nasonia vitripennis. University of Groningen. https://doi.org/10.33612/diss.102037680
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Endogenous timing mechanisms organise molecular, physiological and behavioural processes and synchronize them to external stimuli. Daily light-dark cycles entrain the core circadian clock of most organisms and leads to an internal representation of the environmental light condition which synchronizes peripheral secondary clocks and following processes. A circadian phase of approximately 24 h adjusts to the external phase of 24 h and resets to it. Although there is no change in the external cycle length, photoperiod changes over the year and this pattern changes with latitude. Equatorial regions show nearly no annual variation in photoperiod which changes towards the poles. In polar regions variation occurs from constant darkness in winter to constant light in summer. These extreme photoperiods are more shallow at temperate regions but still show annual variation of several hours. That fluctuation in photoperiod goes along with variation in temperature and is followed by resource availability, necessary for survival and reproduction of higher tropic organisms. Therefore, annual variation of environmental conditions (temperature, nutrition supply) requires adaptation of organisms that depend on latitude. Robust and accurate seasonal timing mechanisms are needed which induce species specific survival strategies to overcome unfavourable conditions. Therefore it seems likely to assess time of year by measuring photoperiod, a solid and recurring external cue, to anticipate seasonal changes. The circadian system provides a daily timing device that conceptually be involved in measuring day length. The question is how the circadian and the annual timing mechanisms influence each other and how these systems adapt to different environmental conditions. Various strategies can be divers and species specific, as described by others.
We studied Nasonia vitripennis, a parasitoid wasp with a world-wide distribution range showing a strong seasonal response of larval diapause induces by short photoperiods and a robust circadian period under constant conditions. We have investigated lines collected from different geographical locations in Europe, one originating from Oulu, Finland (65°3’40.16’’N, 25°31’40.80’’E; northern line) and one from Corsica, France (42°22’40.80’’N, 8°44’52.80’’E, southern line; Paolucci et al. 2013). With these lines we performed comparative studies to get a better understanding of the effect of photoperiod on the circadian system and the mechanisms that drive adaptation of the biological clock to seasonal environments. The aim of this thesis is not to provide extensive proof of evolutionary adaptation to latitude, but rather to provide novel insights and provide more detailed pieces of chronobiological evidence on how possible mechanisms of adaptation might work in nature. We determined differences between the lines in circadian light resetting, its effect on survival and photoperiodism and circadian period. Further molecular studies on light reception of the circadian system were conducted to provide more insight in how the hymenopteran circadian clock might entrain to the external light-dark cycle.
We performed locomotor activity recording to determine free-running period (Chapter 2) and established phase response curves under various light durations and intensities to determine circadian light sensitivity (Chapter 3). Our results show a longer free-running period and a higher light sensitivity in the northern line compared to the southern one. We propose that the longer free-running period is necessary due to the involvement of the circadian system in diapause regulation, to induce diapause at longer photoperiods and herewith to
2013). This would match the increasing critical photoperiod at increasing latitudes shown in
Nasonia (Paolucci et al., 2013). Furthermore, we hypothesise that the northern line is more light
sensitive to keep daily circadian organisation in long natural photoperiods due to strong light resetting. General oscillator theory provides a phase-period rule, which might be able to explain the slower clock in the northern line and its functional involvement in changes of the critical photoperiod. Longer free-running periods, deviating more from 24 h, will result in a shift of the phase angle of entrainment and hence a shift in the exposure of the light sensitive window involved in diapause regulation.
While longer circadian periods might accommodate a fitness enhancing latitudinal adaptation in diapause timing, according to the circadian resonance fitness hypothesis it is also expected to have adverse effects on adult survival when the deviation from 24-h increases (Ouyang et al. 1998; Wyse et al. 2010). The circadian resonance fitness hypothesis predicts fitness costs in terms of reduced survival due to larger daily phase shifts needed for daily circadian entrainment (Pittendrigh and Minis 1972). From this, the expectation follows that the more the circadian period deviates from 24-h, the more longevity is reduced. We tested this longevity hypothesis in a range of environmental light-dark periods (T-cycles) and photoperiod combinations (Chapter 2). Higher longevity was expected to occur in T-cycles close to free-running period, but we did not observe a reduction in longevity in our northern and southern lines with the light-dark period deviating from internal circadian period. These results may be understood by the strong circadian light response we have established in Nasonia, especially in the northern line (Chapter 2 & Chapter 3). We hypothesize that the higher light sensitivity enables a stronger light resetting to maintain a fixed phase angle of behavioural entrainment, independent of intrinsic circadian period. This fixed phase angle of entrainment might be the reason that survival is not reduced when large deviations between circadian period and environmental period may evolve to optimize photoperiodic adaptation.
To understand how our previous results about daily circadian properties and light sensitivity can explain differences in seasonal timing processes, we applied a partial Nanda-Hamner protocol to measure diapause induction under different T-cycles and photoperiods (Chapter 4). We aimed to explain differences in diapause response in a northern and a southern line by studying differences in circadian entrainment properties in a combination of different T-cycles and photoperiods. Our results confirm that the critical photoperiod at which Nasonia females change from producing non-diapausing larvae to diapausing larvae is different for the northern line (longer free-running period) and the southern line (shorter free-running period than the northern line). The northern line was diapausing in all T-cycles when photoperiods were short, whereas diapause in short photoperiod only occurred in the southern line when T-cycles were close to 24 h. Due to the differences of the phase-period relationship (Chapter 2) in the northern and southern lines and the results of the diapause induction experiments (Chapter 4), we suggest that our results are best explained by an external coincidence timing model rather than the more complex internal coincidence timing model as proposed by Saunders (1974, Chapter 4). The higher light sensitivity in the northern line seems to result in a flatter phase-period relationship under a rage of T-cycles while the lower light sensitivity of
adaptation in Nasonia could indeed be causally linked to differences in properties of the circadian system. Our findings indicate that differences in circadian light sensitivity and variation in circadian free-running period might be a sufficient mechanism to explain adaptation to latitude in nature. This hypothesis, however, remains to be tested in natural populations with original genetic variation.
We have shown strong evidence that circadian light resetting is critical for adaptive circadian entrainment of Nasonia and seasonal timing of diapause, but the molecular mechanism by which the circadian system of Nasonia, or other hymenopteran insects, entrains to light is still unknown. hymenopteran do not encode for the photo-sensitive variant of the clock protein Cryptochrome, as observed in Drosophilids and other insect species; hymenoptera encode for the mammalian-like photo-insensitive Cryptochrome. The mammalian clock resets is induced by light through immediate early gene induction of per1 and subsequently per2 through a CREB signalling pathway (Albrecht et al. 1997; Shearman et al. 1997; Shigeyoshi et al. 1997; Travnickova-Bendova et al. 2002). To identify and locate the circadian light resetting mechanism of the clock work of Nasonia, we tested light induced immediate early gene induction of canonical clock genes (Chapter 5). Additionally, we measured opsin gene expression levels to identify possible mechanism by which the north-south difference in light sensitivity might be explained (Chapter 5). Our results do not support the idea of circadian light resetting by immediate early gene induction of clock genes. Also the opsin measurement did not provide further insight in the underlying processes and by this critical differences between the lines. Further research is required to elucidate circadian light resetting mechanisms in hymenoptera. Once mapped, we hypothesise that the genes involved in the molecular mechanisms of circadian light reception will provide a substrate for latitude related selection pressure enabling the circadian system to change the photoperiodic response with increasing latitude.
Endogene timingsmechanismen organiseren moleculaire, physiologische en gedragsprocessen en synchroneren deze processen met externe stimuli. Dagelijkse licht-donker cycli entraineren de circadiane klok van vrijwel alle organismen. Lichtinformatie biedt het hart van dit system een representatie van tijd van de dag, welke vervolgens gebruikt wordt om perifere en daaropvolgende processen te synchroniseren. De circadiane cyclus past zijn periode van ongeveer 24 uur aan zodat deze overeenkomt met de 24-uurs periode van de externe cyclus. Daarbij wordt de fase van de circadiane cyclus gecorrigeerd om een gewenste fasehoek met de externe 24-uurs cyclus te realiseren. Hoewel er geen verandering plaatsvindt in de periode van de externe cyclus is fotoperiode afhankelijk van breedtegraad. De jaarlijkse variatie in fotoperiode is het grootst op de polen en is nauwelijks aanwezig op gebieden rond de evenaar. Fotoperiode op poolgebieden varieert van constant donker in de winter tot constant licht in de zomer. Deze extreme fotoperioden vlakken af richting meer gematigde gebieden, maar ook hier treden nog steeds jaarlijkse variaties in fotoperiode op van enkele uren. Die fluctuatie in fotoperiode gaat gepaard met variatie in temperatuur. Deze variatie op zijn beurt beïnvloedt beschikbaarheid van voedsel en andere hulpbronnen, welke cruciaal zijn voor voorplanting en overleving. Daarom vragen jaarlijkse variaties in omgevingsfactoren (temperatuur, voedselbeschikbaarheid) specifieke overlevingsstrategiën van een organisme, welke afhankelijk zijn van waar op de wereld het betreffende organisme zich bevindt. Om goed om te kunnen gaan met de nadelige condities die dit soort jaarlijkse veranderingen met zich mee brengen, zijn nauwkeurige en robuuste tijdsinschattingsmechanismen op seizoensniveau nodig. Het is daarom aannemelijk dat organismen de tijd van het jaar in kunnen schatten aan de hand van gemeten fotoperiode, een betrouwbaar en steeds terugkerend signaal, om zich voor te kunnen bereiden op seizoensgebonden veranderingen in de omgeving. De vraag is wat precies de wisselwerking is tussen circadiane en circannuele tijdswaarnemingssystemen, en hoe deze systemen zich aanpassen aan verschillende omgevingscondities. Het is al bekend dat zulke aanpassingsstrategieën zeer divers en soortspecifiek zijn.
Wij hebben Nasonia vitripennis bestudeerd, een parasitoïde wesp die over de hele wereld te vinden is. Deze wesp laat een sterke seizoensgebonden respons zien in de vorm van larvale diapause geïnduceerd door korte fotoperioden, en heeft een robuuste circadiane periode onder constante condities. We hebben genetische lijnen bestudeerd, verzameld uit verschillende geografische locaties in Europa: een lijn uitt Oulu, Finland (65°3’40.16’’N, 25°31’40.80’’E; noordelijke lijn) en een lijn uit Corsica, Frankrijk (42°22’40.80’’N, 8°44’52.80’’E, zuidelijke lijn; Paolucci et al. 2013). We hebben vergelijkende studies ondernomen met deze twee lijnen om een beter begrip te ontwikkelen van het effect van fotoperiode op het circadiane systeem, en de mechanismen die verantwoordelijk zijn voor aanpassingen van de biologische klok aan seizoensgebonden omgevingsveranderingen. We hebben verschillen vastgesteld tussen deze lijnen met betrekking tot circadiane klokverschuivingen door licht, de invloed van de klok op overleving, fotoperiode en circadiane periode. Daarnaast hebben we verder onderzoek betreffende verwerking van lichtinformatie door het circadiane systeem uitgevoerd.
We hebben opnames gemaakt van locomotorische ativiteit om de periode in vrijloop vast te stellen (Hoofdstuk 2) en we hebben fase-respons curves vastgesteld onder verscheidene lichtduren en intensiteiten om de lichtgevoeligheid van het circadiane systeem te bepalen
lichtgevoeligheid zien voor de noordelijke vergeleken met de zuidelijke lijn. Wij stellen voor dat de langere periode in vrijloop nodig is vanwege betrokkenheid van het circadiane systeem bij de regulering van diapause, zodat diapause al bij langere fotoperioden plaatsvindt om de lange wintercondities in noordelijke habitats te kunnen overleven (Hut and Beersma 2011; Hut et al. 2013). Dit zou overeenkomen met de toenemende kritische fotoperiode naarmate de breedtegraad ook toeneemt, zoals eerder aangetoond voor Nasonia (Paolucci et al., 2013). Verder stellen wij de hypothese op dat de noordelijke lijn lichtgevoeliger is om dagelijkse circadiane organisatie in stand te houden tijdens lange fotoperiodes, met behulp van sterke circadiane licht respons. De fase-periode regel zou variatie in circadiane periode en de betrokkenheid hiervan bij veranderingen in de kritische fotoperiode kunnen verklaren; deze regel stelt dat langere periodes in vrijloop, die meer afwijken van 24 uur, resulteren in een verschuiving in de fasehoek van entrainment. Daarbij zou de hogere lichtgevoeligheid van de noordelijke lijn ervoor zorgen dat deze lijn een groter bereik van entrainment heeft dan de zuidelijke lijn.
Hoewel langere circadiane periodes een 'fitness'-bevorderende breedtegraadsafhankelijke adaptatie in de timing van diapause kunnen bevorderen, kan tegelijkertijd verwacht worden volgens de ciradiane resonantie 'fitness' theorie dat langere ciracadiane periodes nadelige effecten hebben naarmate de afwijking ten opzichte van 24 uur toeneemt (Ouyang et al. 1998; Wyse et al. 2010). De circadiane resonantie 'fitness' theorie voorspelt 'fitness' kosten in de vorm van verlaagde overlevingskansen, doordat een biologische klok die meer afwijkt van 24 uur elke dag een grotere faseverschuiving nodig heeft om geëntraineerd te blijven (Pittendrigh and Minis 1972). Vandaar de verwachting dat hoe meer een circadiane periode afwijkt van 24 uur, hoe korter de levensduur. We hebben deze levensduurhypothese getest onder verschillende combinaties van licht-donker periodes (T-cycli) en fotoperiodes (Hoofdstuk 2). We verwachtten een langere levensduur te zien bij T-cycli dichterbij de periode in vrijloop, maar we vonden geen afname in levensduur in de noordelijke en zuidelijke lijnen. Deze resultaten kunnen verklaard worden door de sterke circadiane lichtrespons (het opnieuw instellen van het circadiane systeem met een enkele lichtpuls) die we vooral gemeten hebben in de noordelijke lijn (Hoofdstuk 2 en Hoofdstuk 3). We stellen de hypothese voor dat de hogere lichtgevoeligheid deze wesp in staat stelt om een sterke circadiane lichtrespons te laten zien opdat een vaste fasehoek van entrainment kan worden behouden, onafhanelijk van de periode in vrijloop. Deze vaste fasehoek van entrainment zou de reden kunnen zijn dat de levensduur niet afneemt terwijl grote afwijkingen tussen de periode in vrijloop en de periode van de licht-donker cyclus geëvolueerd zijn om fotoperiodieke adaptatie te optimaliseren.
Om te begrijpen hoe bovengenoemde resultaten over dagelijkse circadiane eigenschappen en lichtgevoeligheid verschillen kunnen verklaren in seizoensgebonden timingsprocessen, hebben we het Nanda-Hammer protocol toegepast om diapause-inductie te meten onder verschillende T-cycli en fotoperioden (Hoofdstuk 4). Het doel was hier om verschillen in de diapause-respons te verklaren in een noordelijke en zuidelijke lijn, door verschillen in de eigenschappen van circadiane entrainment in combinatie met verschillende T-cycli en fotoperioden te bestuderen. Onze resultaten laten zien dat de kritische fotoperiode, wanneer
lijn (kortere periode in vrijloop dan de noordelijke lijn). De noordelijke lijn produceerde diapause-larvae onder alle T-cycli bij bepaalde korte fotoperioden, terwijl de zuidelijke lijn alleen diapause-larvae produceerde bij T-cycli dichtbij 24 uur en bij bepaalde korte fotoperioden. Dit is een sterke aanwijzing dat seizoensgebonden breedtegraadsafhankelijke adaptatie in Nasonia veroorzaakt kan worden door verschillen in eigenschappen van het circadiane systeem. Verschillen in lichtgevoeligheid tuseen beide lijnen, variatie in periode in vrijloop en circadiane fase zouden deze resultaten mogelijk kunnen verklaren. De hogere lichtgevoeligheid in de noordelijke lijn lijkt te leiden tot een vlakkere fase-periode relatie onder een verscheidenheid aan T-cycli, terwijl de lagere lichtgevoeligheid van de zuidelijke lijn resulteert in een stijlere helling van de fase-periode relatie zoals verwacht wordt aan de hand van de fase-periode regel. Vanwege de verschillen in de fase-periode relatie (Hoofdstuk 2) in de noordelijke en zuidelijke lijnen en de resultaten van de diapause experimenten (Hoofdstuk 4), suggereren wij dat onze resultaten het best verklaard kunen worden door een extern toevalligheidstiming model in plaats van het meer complexe interne toevalligheidstiming model zoals voorgesteld door Saunders (1974, Hoofdstuk 4).
We hebben sterk bewijs gepresenteerd dat het herinstellen van de circadiane klok door licht van groot belang is voor adaptieve circadiane entrainment van Nasonia en de seizoensgebonden timing van diapause, maar het moleculaire mechanisme waarmee het circadiane systeem van Nasonia of andere vliesvleugelige insecten entraineren aan licht is nog steeds niet bekend. In tegenstelling tot Drosophilidae, encoderen vliesvleugeligen de lichtgevoelige klokproteïne Cryptochrome niet; zij encoderen het zoogdierachtige Cryptochrome dat niet gevoelig is voor licht. De klok van zoogdieren reageert op licht door 'immediate early gene' inductie van per1 en vervolgens per2 via een CREB signaalroute (Albrecht et al. 1997; Shearman et al. 1997; Shigeyoshi et al. 1997; Travnickova-Bendova et al. 2002). Om het circadiane lichtherstellingsmechanisme van de klok van Nasonia te identificeren en te lokaliseren, hebben we lichtgeïnduceerde 'immediate early gene' inductie getest van canonieke klokgenen (Hoofdstuk 5). Daarbij hebben we opsine-gen expressie gemeten om het mogelijke mechanisme te identificeren waarmee het verschil in lichtgevoeligheid tussen de noordelijke en zuidelijke lijnen zou kunnen worden verklaard (Hoofdstuk 5). Onze resultaten ondersteunen het idee van circadiane aanpassing door licht door 'immediate early gene' inductie van klokgenen niet. Ook de opsin-metingen biedden geen verder inzicht in de onderliggende processen en hiermee belangrijke verschillen tussen de twee lijnen. Verder onderzoek is nodig om mechanismen van circadiane klokverschuivingen door licht te verklaren in vliesvleugeligen.
Time flies! Well, depends ;). After 6.5 years I am happy, proud, exhausted and still surprised to be able to close this chapter of my life with this piece of work and a PhD degree! But I couldn’t have done this without massive support by a big group of people.
First of all, I would like to thank my supervisors Roelof Hut and Domien Beersma. I enjoyed the stimulating discussions, the meetings and the exchange of opinions about our research a lot. Thank you for your enthusiasm, your interest and support. Roelof, your passion for science and chronobiology has always been very inspiring and infectious. I am deeply grateful that you believed in the project and me as a scientist and never lost patience with me (at least not that you have shown it to me ;) )! Domien, you do not force your opinion on anyone, but you have always been interested and when asked, you always were up for a good advice. With your calm way, you could even restrain my nervousness and stress level before presentations. Thank you a lot for that as well.
Many thanks to the assessment committee (Bregje Wertheim, Jeff Harvey, Bambos Kyriacou) for taking the time to read and approve this thesis and to the PhD Examining Committee (Barbara Helm, Jeff Harvey, Bambos Kyriacou, Peter Meerlo, Ralf Stanewsky) for accepting to take part of the PhD graduation ceremony.
My project was part of the European Initial Training Network “INsecTIME” and I feel very privileged that I could be part of a group of wonderful personalities and great scientists! Our meetings and conversations have been very inspiring, we have learnt a lot from each other and had a great time together.
My dearest paranymphs Giulia & Meghan, I couldn’t imagine this phase of my life without you! You are my ladies in crime! I’m very thankful for the time we spent together in Groningen, the fun, the frustration, the parties and drama. You have become my best friends and although now there is quite some distance between us, thanks to modern communication technology there is not a week without us communicating somehow. But of course, I miss our girls nights, weekend trips and lunch, talking a mix of science, Dutch singularities, politics, reality TV shows, feminism, students and many other things. Thank you for your friendship and the many great experiences we have shared together!!
A giant thank you to the entire Chrono Lab! Namely Vincent, Tom, Sjaak, Moniek, Simone, Renske, Emma, Marijke, Menno, Peter, Laura, Lauren, Sjoerd. You are amazing! Although my insect project didn’t entirely match with your work, you always showed great interest in my work and provided helpful advices. Besides work, it was fun have a little chit chat in the hallway or going for a Friday afternoon/evening/night borrel, traveling to conferences or having a nice sushi dinner together. I really enjoyed the time we spent together! Special thanks to Vincent, my first friend in the Netherlands. Tom, my Dutch translator with a most wonderful dry humour and Renske who hosted me so often when I came back to Groningen to work with Roelof or when I needed somebody for a quick Dutch-English translation or a companion for a glass of wine ;). I really appreciate your friendships!
Thanks to the Nasonia Lab! Anna and Silvia for teaching me the handling with the animals and for helping out when needed, thanks Leo and Louis for interesting discussions and helpful
