Photoperiod response corresponds to different circadian entrainment properties in northern and southern Nasonia vitripennis lines

doi:10.21203/rs.3.rs-2880228/v1

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Photoperiod response corresponds to different circadian entrainment properties in northern and southern Nasonia vitripennis lines

https://doi.org/10.21203/rs.3.rs-2880228/v1

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published 18 Oct, 2023

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The circadian clock times physiological and behavioural processes and resets on a daily basis to synchronize with the environment. The involvement of the circadian clock in photoperiodic time measurement synchronising annual rhythms is still under debate and different models have been proposed explaining their integration. Insects overcome unfavourable conditions in diapause, a form of dormancy. A latitudinal cline in diapause induction in the parasitoid wasp Nasonia vitripennis as well as a difference in circadian light sensitivity between north and south provide us with additional evidence that the circadian system of Nasonia is involved in photoperiodic time measurement and that circadian adaptation is a potential mechanism driving latitudinal adaptation in photoperiodism. We tested diapause induction in a range of T-cycles and photoperiods and found diapause induction in short photoperiods in all T-cycles in the northern line but in the southern line diapause only occurred in T-cycles close to 24 h. Due to a lower light sensitivity in the southern line, a wider distribution of phase angles of entrainment can be expected at a specific T-cycle duration, while the range of entrainment will decrease. Taking these oscillator properties into account, our data can be explained by an external coincidence model involving a single oscillator with a light-sensitive phase that drives annual timing of diapause in Nasonia vitripennis.

Nasonia

photoperiodic response

latitude

seasonality

circadian clock

partial Nanda-Hamner

external coincidence timer

diapause

Hymenoptera

photoperiodism

1.1. Seasonality, photoperiodism and the circadian system

Organisms exist in a dynamic environment, with periodically occurring daily and seasonal changes. It is necessary for survival to initiate physiological processes in anticipation of upcoming seasonal changes. Therefore, photoperiodic time measurements evolved, which determine the time of year by measuring day length (Danilevskii 1965, Hut et al. 2013). In insects, seasonal changes have led to adaptive temporal organisation of seasonal growth, reproduction and diapause (dormancy). Responses to seasonal changes in day length drive seasonal physiology (Marcovitch 1923). This requires a neurophysiological system that measures either night length (scotoperiod), day length (photoperiod) or both. The sensitive period in which an organism will respond to this photoperiodic stimulus either occurs in the life cycles of the organism itself (inducing adult diapause as in Drosophila melanogaster, Saunders et al. 1989) or in the parental generation which leads to diapause in egg or larval state (larval diapause in Nasonia vitripennis, Saunders 1965a, 1965b). It has been studied intensively whether the night or the day length is the crucial component by inducing diapause (see review by Saunders (2013)) and it seems that in many tested insect species the duration of darkness is the determining signal (Saunders 1973), although the duration of the light phase as critical signal has also been found (Saunders 1987). In Nasonia, as in some other insect species, seasonal timing involves the circadian system (Saunders 1968, 1974, 1990), but in other species proof of circadian involvement seems absent (Pittendrigh et al. 1970, Pittendrigh and Minis 1971, Lees 1990). In mammals, a seasonal timing mechanism requires the involvement of the circadian system and circadian clock genes (Dardente et al. 2010, Masumoto et al. 2010). Although light is the main inductive stimulus, also temperature, food availability, population density or humidity can influence seasonal response (Saunders 1966, 1970; Tauber et al. 1986; Hodkova and Socha 1995; Christiansen-Weniger and Hardie 1999; Saunders et al. 2002).

A model explaining photoperiodic time measurement and the involvement of a circadian clock was firstly proposed by Bünning (1936). He proposed a dual-phasic oscillator with a frequency of approximately 24 h, consisting of a photophil phase of 12 h that required light and a scotophil phase of also 12 h requiring darkness. A short day response, for example diapause, is expected when light only occurs during photophil whereas a long day response will occur when the light is extended into scotophil phase. Thus, Bünning combined the daily time measurement of the circadian clock with the measurement of the darkness duration to form an internal representation of day length required for the seasonal response. An alternative system not involving a self-sustainable oscillator is the hourglass model (Lees 1973). It requires a daily stimulation of the system by an external light-dark cycle. The system measures either the length of the light or dark phase by a homeostatic process which is reset every day, and crosses a threshold after a critical duration of the light or dark phase. Bünning’s original oscillator theory was taken further by Pittendrigh (Pittendrigh and Minis 1964, Pittendrigh 1966) by describing an external coincidence model which states the occurrence of short day response (e.g. diapause) when a single oscillator’s light-sensitive phase coincides with environmental darkness and a long day response when the light-sensitive phase coincides with light. In the internal coincidence model, Pittendrigh (1972) proposed two oscillators: one coupled to dawn and one to dusk. Their phase angle difference forms an internal representation of day length and determines seasonal status of the organism. In addition, the internal and external coincidence models, describing the involvement of the circadian system in photoperiodism, may lead to different predictions for latitudinal selection pressure on circadian properties like free-running period and light sensitivity (Hut and Beersma 2011).

1.2. Critical photoperiod and latitudinal cline

As mentioned above, insects can survive unfavourable conditions by going into diapause. Depending on the species, diapause can occur at different stages of the life cycle (Tauber et al. 1986) and usually occurs when photoperiod decreases to a specific threshold: the critical photoperiod (CPP). Seasonal variation in temperature and day length increases with distance to the equator, while the average environmental temperature decreases (Hut et al. 2013). Together this resulted in the hypothesis that CPP should increase with latitude to form a so-called latitudinal cline. Data sets from many insect species confirmed a latitudinal cline in CPP; insect populations from higher latitudes show diapause at longer photoperiods than their relatives from lower latitudes (Danilevskii 1965; Hut et al. 2013). Paolucci et al. (2013) showed in an extensive study a latitudinal cline in CPP, where northern Nasonia vitripennis populations have longer CPP than the southern populations. Nasonia shows a distinct short photoperiod maternal response which induces diapause in the offspring larva (Saunders 1965, 1966). In addition, Nasonia adults expresses a strong and stable circadian activity rhythm with a clear diurnal pattern (Bartossa et al. 2013, Floessner et al. 2019). These both characteristics and its global occurrence are requirements that make Nasonia an appropriate study species for seasonal and circadian environmental adaptation. Furthermore, quantitative trait locus (QTL) analysis discovered two genomic regions involved in diapause induction (Paolucci et al. 2016). These regions (on chromosome 1 and 5) encode for three important clock genes period, cycle and cryptochrome. Further analysis of the period gene showed latitudinal variation of mainly two haplotypes, one with higher frequency in northern populations and the other with higher frequency in southern populations (Paolucci et al. 2016). Additionally, we have determined higher light sensitivity and longer circadian free-running periods in a northern Nasonia line compared to a southern line (Floessner et al. 2019).

Latitudinal clines are seen in many biological aspects and are usually considered to be an adaptive evolutionary response to a latitudinal environmental gradient (Hut et al. 2013). They can be used to trace evolutionary selection pressures for specific processes and may therefore be informative to find essential elements (genes) in physiological pathways of interest.

1.3. General aim

Here we aim to extend our knowledge about the involvement of the circadian system in photoperiodic response to the mechanism that drives latitudinal adaptation of Nasonia vitripennis by exposing a northern and a southern line to a partial Nanda-Hamner protocol. The full Nanda-Hamner protocol uses a wide combination array of photoperiods and cycle durations (Tcycles; Nanda and Hamner 1958). Briefly, when a photoperiodic response occurs under 24 h cycles (or multiples thereof), but not under non-24 h T-cycles, an involvement of the circadian system in photoperiodic response is concluded. Those “positive” responses were measured for example in Nasonia vitripennis, (Saunders 1968, 1974) and Drosophila melanogaster, (Saunders 1990). But also “negative” results have been reported in the Pink bollworm Pectinophora gossypiella (Pittendrigh et al. 1970, Pittendrigh and Minis 1971) or the pea aphid Acyrthosiphon pisum (Lees 1990) showing a non-circadian response or an hourglass timing system (Saunders 1974). The full Nanda-Hamner protocol in Nasonia provided evidence for the involvement of a circadian internal coincidence timing system (Saunders 1974). This finding allowed us to define a partial Nanda-Hamner protocol with a limited range of T-cycles around 24 h, aimed to distinguish differences between a northern and southern line of Nasonia vitripennis, in which a latitudinal cline in critical photoperiod, in circadian period, and in circadian light sensitivity have been described previously (Paolucci et al. 2013, Floessner et al. 2019). When the circadian system is involved in photoperiodism, then the north-south differences in circadian light sensitivity between these lines should also result in observable differences in diapause responses to a partial Nanda-Hamner protocol, thus providing additional evidence for circadian involvement in photoperiodism in Nasonia vitripennis.

2.1. Experimental lines

Experiments were performed with two Nasonia vitripennis isofemale lines that had been established from single females originating from Oulu, Finland (65°3’40.16’’N, 25°31’40.80’’E) and Corsica, France (42°22’40.80’’N, 8°44’52.80’’E; Paolucci et al. 2013). We are specifically using these two lines, “northern line” (Oulu) and “southern line” (Corsica), because they were described before to differ in circadian light sensitivity (Floessner et al. 2019). Both lines were reared in temperature and humidity controlled climate chambers at 20° C (± 1°C), 50–55% RH, and a light-dark cycle of 16h light: 8h dark (LD16:8). The wasps used during the experiment were F1 generations of individually housed females, supplied with two Calliphora spp. pupae as hosts.

2.2. Entrainment period and test period

We used a partial Nanda-Hamner protocol to distinguish between photoperiodic responses in northern and southern lines. The experimental set up follows closely Saunders protocol that he applied during the T-cycle measurements of Nasonia vitripennis (Saunders 1968, 1974) to enable reliable comparisons. The light regime was designed to distinguish night length driven responses from day length driven responses (Vaze and Helfrich-Förster 2016). In our partial Nanda-Hamner protocol, groups of wasps were placed under various light-dark conditions using 5 different light-dark cycle durations (or Tcycles, of T-18 h, T-21 h, T-24 h, T-27 h, T-30 h) and within each T-cycle four different night lengths of 5, 8, 11 and 14 h and a variable number of hours in light adding up to the required T-cycle (Fig. 1). The light regime for each group was maintained throughout the entire experiment and did not change. During the entrainment period (day 1 to day 16) and test period (day 16 to day 18) the wasps were exposed to the experimental light-dark regimes (Fig. 1). For each experimental group we prepared three mass culture vials per line containing ~ 30 females, ~ 5 males and ~ 30 hosts. For each LD-cycle group there were 33 parasitized pupae on average (range 22–64). On day 8 fresh host pupae were added during the light phase to feed the wasps.

For the test period (day 16 to day 18) individual females, 25 per experimental group, were transferred into acrylic test tubes and supplied with two fresh Calliphora spp. pupae as hosts. Females were removed 48 hours later (in the end of the light phase of day 18) and the test tubes transferred into constant darkness for 3 more weeks so the eggs could develop into diapausing larvae or develop into pupae. The experiment was performed in light-tight boxes (23 x 14 x 32 cm) at 18°C (± 1°C). Each light-tight box was illuminated with one LED light source (Neutral White 4000K PowerStar, Berkshire) of 2.1 · 10¹⁵ photons·cm^-2·s^-1.

2.3. Diapause assessment

To score diapause response, the two host pupae in each test tube were opened and the status of the offspring was assessed. Diapausing offspring was hold in a larval state whereas developing offspring had developed into adults in the meantime of 3 weeks. A host pupa was counted as ‘diapausing’ when ≥ 50% of the progeny was in diapause, in the vast majority the offspring was either entirely diapausing or entirely developing (non-diapausing). Host pupae that were not parasitized were excluded from further calculations. For each light cycle, the results were calculated as the percentage of host pupae containing diapausing offspring during the test period.

Both lines showed transitions from non-diapausing offspring to diapausing offspring (Fig. 2). Comparing diapause incidence within lines and between the different T-cycles, we noticed in the northern line that for all T-cycles a steep transition from non-diapausing offspring to diapausing offspring occurred at longer photoperiods (Fig. 2A, C), although 100% diapause was not reached in T-18 h, T-27 h and T-30 h (Fig. 2A, C). In T-18 h the critical photoperiod was the shortest of all T-cycles, followed by T-21 h. T-24 h and T-27 h showed a nearly identical CPP and in T-30 h the CPP was the longest. In summary, the northern line showed diapause response at all T-cycles.

In the southern line, diapausing offspring was only observed in T-21 h and T-24 h. T-21 h expressed a shorter CPP than T-24 h (Fig. 2B, D). The other T-cycles resulted for all LD regimes in less than 50% diapause. In T-30 h we measured 4–12% diapause incidence for all LD cycles (Fig. 2B, D).

Comparing both lines with each other, we see that the northern line responded stronger and with distinct response to the different T-cycle regimes than the southern line. The southern line did not show diapause response when T-cycles deviation from 24 h was large, especially when T was longer than 24 h.

Vaze and Helfrig-Förster (2016) raised the question whether the absolute day length or rather the night length was measured by the photoperiodic system. Therefore, we re-plotted our data also as a function of absolute night length expecting that when absolute night length is measured, the curves would superimpose. A logistic regression model was used within each strain and day length or night length analysis to determine significant differences in inflection points between T-cycles, using identical slopes. For the northern strain, the day and night length analyses showed a highly significant dependency of diapause on day length, when different constants were estimated for each T-cycle treatment (Fig. 2A&C; n = 24, df = 18, dev.=103.79, p < 0.0001). For the southern strain, the day and night length analyses showed a highly significant dependency of diapause on day length, when different constants were estimated for each T-cycle treatment (Fig. 2B&D; n = 24, df = 18, dev.=113.28, p < 0.0001). The variation in inflection points for each T-cycle did not differ within each strain between the day length and night length analysis (Northern strain: sd_day=2.82, sd_night=2.24; F_4,4=1.59, p > 0.33; Southern strain: sd_day=4.05, sd_night=4.21; F_4,4=1.08, p > 0.47). Thus, diapause incidence plotted against night length (Fig. 2C, D) does not show better superposition than when diapause is plotted against day length (Fig. 2A, B), suggesting that both day length and night length influence diapauses induction in these Nasonia strains.

Our results confirm Saunders’ data of Nasonia diapause responses in a full Nanda-Hamner landscape (Saunders 1968, 1974). Our partial Nanda-Hamner protocol was not designed to confirm a positive Nanda-Hamner response showing circadian involvement in photoperiodism. Instead, our comparison between the northern and southern line provides additional evidence that latitudinal adaptation in Nasonia may be caused by differences in properties of the circadian system, resulting in adaptive differences in photoperiodic responses. The northern Nasonia line shows in different T-cycles a positive response and variation in CPP; with longer CPP in longer T-cycles and shorter CPP in short Tcycles. These differences became slightly smaller when plotting the data as a function of critical night length, but still the curves did not superimpose. This may indicate that the photoperiodic system in the northern Nasonia line responds to both day length and night length.

In the southern line clear diapause induction just occurred in T-21 h and T-24 h with different CPP that was longer in T-24 h than in T-21 h but lay on top of each other when plotted as a function of critical night length. This suggests that the southern Nasonia line may measure night length rather than day length. The lack of diapause induction in the southern line at T-18 h, T-27 h and T-30 h may indicate that there was no entrainment (the system is not in ‘resonance’), and that light perceived at all phases of the circadian cycle resulted in effective suppression of diapause. This can be considered as evidence that the system does not respond as an hour glass model, where diapause should have occurred in all T-cycles at short photoperiods.

In his complete Nanda-Hamner study, David Saunders used a Nasonia line originating from Cambridge, United Kingdom (52°12’19.213’’N, 0°7’18.541’’E; Saunders 1968, 1974), an intermediate latitudinal location between Oulu, Finland (65°3’40.16’’N, 25°31’40.80’’E) and Corsica, France (42°22’40.80’’N, 8°44’52.80’’E). Re-plotting Saunders results (Fig. 3) from T-cycles similar to cycle lengths that we used, we find similarities to both our northern and the southern data (Fig. 2A, B & Fig. 3). T-16 h, T-21 h, T-24 h, T-28 h show diapause induction at long photoperiods. T-32 h does not show more than 25% diapause induction, similar to results shown by the southern line (Fig. 2B). We conclude that the results of Saunders also support our conclusion since those data show intermediate diapause induction responses when compared to our northern and southern data, while the geographical origin of the Saunders strain was also intermediate to the strains we used.

Saunders collected large data sets when he applied night interruption experiments (Saunders 1970) and the Nanda-Hamner protocol (Saunders 1974). Both experimental approaches led to the conclusion of a circadian based seasonal timing mechanism. Further, Saunders wanted to determine oscillator properties, especially whether internal or external coincidence model drives seasonal timing. At the time, he interpreted his findings as internal coincidence model based on the position of the ascending and descending slope of the peak of the photoperiodic response curve. “…When the photoperiod was increased from 12 h to 14 or 16 h the ‘descending slope‘ of the peaks remained in the same position (at T = 28–32 and at T = 52–56), but the ‘ascending slope’ moved to longer T values in such a way that the maxima became narrower. …. A similar, but opposite trend was observed when the photoperiod was shortened; the ‘ascending slope’ moved steadily to the left, whereas the ‘descending slope’ remained constant, except with the 4 h photoperiod in which a perceptible movement to left was also apparent.“ (Saunders 1974). He connected the ascending slopes with dusk and the descending slopes with dawn and by that he drew the conclusion of an internal coincidence model with a morning oscillator tracking dawn and an evening oscillator tracking dusk (Saunders 1974).

Here we propose an alternative explanation based upon an external coincidence timing model, similar to the photoperiodic timing mechanism located in the mammalian Pars tuberalis (Dardente et al. 2010, Masumoto et al. 2010). Essential for evaluation of the involvement of circadian components in photoperiodic timing in unusual T-cycles is whether the circadian system is able to entrain or not, especially in absence of photoperiodic response as shown in the southern Nasonia line (Fig. 2B, D). In prior experiments phase response curves were conducted of females of the northern and southern lines to light pulses of the same light intensity as used here, where light pulses of 4 h or more resulted in phase shifts of more than 7 h advance or delay (Floessner et al. 2019). This means that both the northern (tau = 26.33 h) and the southern line (tau = 25.01 h) probably entrained to all T-cycles presented here. Assuming that circadian entrainment indeed occurred in both lines under all Tcycles, we consider the difference in light sensitivity of the northern and southern line as a possible explanation for the difference in diapause response. The higher light sensitivity in the northern line should result in a shallower phase-period relationship under a range of T-cycles than would be the case with the southern line with a lower light sensitivity (Floessner and Hut 2017). This means that with increasing duration of the Tcycle, the southern line would show a stronger effect on phase (more ‘leading’) than the northern line. This indeed seems to be the case when activity profiles for the northern and southern lines are considered for T-20 h, T-24 h and T-28 h LD cycles (Floessner et al. 2019). When this difference in phase-period relationship between the northern and southern line is applied to an external coincidence model, we can construct a graphical representation model that summarizes our results (Fig. 4). In this model we assume that diapause is suppressed when a single light sensitive phase of ~ 7 h duration would be exposed to light. This light sensitive phase would be coupled to the circadian system and is entrained around the middle of the light phase (Floessner et al. 2019). This parsimonious model can explain all diapause responses presented here when lower light sensitivity in the southern line (Floessner et al. 2019) results in a reduced range of entrainment and a wider phase angle of entrainment range (Floessner and Hut 2017) when compared to the northern line (Fig. 4). The narrower range of phase angle of entrainment in the northern line, resulting from their higher light sensitivity, would then lead to a narrower phase distribution of the light sensitive phase, and hence more similar responses in maintaining diapause at shorter photoperiods at all T-cycles applied (Fig. 4). The wider phase distribution in the southern line, due to their lower circadian light sensitivity, would therefore result in maintenance of diapause only in those T-cycles with a period relatively close to the intrinsic circadian period of that line.

Our ‘external coincidence - phase angle of entrainment’ (EX-PA) model seems in line with the interpretation by Vaze and Helfrig-Förster (2016) that a tight range of phase angle of entrainment may indicate either a weak or dampened oscillator that can be easily entrained by light, or a strong oscillator that can be easily entrained because of a high response/sensitivity to light. Under entrained conditions, these two options can only be distinguished by an independent measure of oscillator strength, perhaps through establishing the robustness of activity rhythms, and by measuring the strength of the circadian light responses. Both measures, robustness of activity profiles and strength of circadian light resetting, seem to indicate that Nasonia has a strong circadian oscillator with strong circadian light resetting, especially in the northern line (Floessner et al. 2019). As a next step, it would be interesting to see to what extent our EX-PA model can explain the full extent of the photoperiodic landscape model as measured by Saunders (1974).

To further support our EX-PA model, we would need better confirmation on the phase angle of entrainment under various T-cycles and we would need to increase our understanding of the system using a wider range of photoperiods and T-cycles applied to a wider range of Nasonia strains. Given the results presented here, we draw the preliminary conclusion that the different diapause responses in our northern and southern lines can be explained (at least partly) by an external coincidence timing model while taking into account the higher circadian light sensitivity in the northern line. This interpretation indicates that variation in circadian light sensitivity, together with adaptation in circadian period, may form the basis for latitudinal adaptation in photoperiod driven seasonal diapause response.

Funding: This research was funded by the Marie Curie Initial Training Network programme INsecTIME (Grant number PITN-GA-2012-316790).

Acknowledgments: We thank Drs. David Saunders, William Bradshaw and Christina Holzapfel for valuable comments to the manuscript. Drs. Charlotte Helfrich-Förster and Kaustubh Vaze for their advice and scientific discussions.

Conflicts of Interest: The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

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published 18 Oct, 2023

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Photoperiod response corresponds to different circadian entrainment properties in northern and southern Nasonia vitripennis lines

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Abstract

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1. Introduction

1.1. Seasonality, photoperiodism and the circadian system

1.2. Critical photoperiod and latitudinal cline

1.3. General aim

2. Materials and Methods

2.1. Experimental lines

2.2. Entrainment period and test period

2.3. Diapause assessment

3. Results

4. Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1