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Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: A review of current understanding
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Journal of Insect Physiology 53 (2007) 869–876 www.elsevier.com/locate/jinsphys
Review
Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: A review of current understanding Stephen J. Simpsona,b,, Gabriel A. Millera,b a
School of Biological Sciences, The University of Sydney, Heydon-Laurence Building A08, NSW 2006, Australia b Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Received 30 April 2007; received in revised form 21 May 2007; accepted 24 May 2007
Abstract Desert locusts demonstrate pronounced density-dependent polyphenism: a complex suite of traits shifts over the lifetime of an individual in response to crowding or isolation. These changes also accumulate across generations through a maternal effect. Female desert locusts alter the developmental trajectory of their offspring in response to their own experience of crowding. The mother possesses a memory of both the recency and extent of crowding and shifts the phase state of her hatchlings accordingly. Extensive experimental work has shown that offspring behaviour is controlled by a low molecular weight, polar compound (or compounds) released from the mother’s accessory glands. The chemical identity of this agent is not yet known. r 2007 Elsevier Ltd. All rights reserved. Keywords: Schistocerca gregaria; Maternal inheritance; Phase change; Locust; Epigenetic effect
Contents 1. 2. 3. 4. 5.
The maternal control of phase state in the desert locust . . Transmitting gregarious characteristics across generations . Transmitting solitarious characteristics across generations . The nature of the maternally produced gregarizing agent . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. The maternal control of phase state in the desert locust The desert locust, Schistocerca gregaria, demonstrates an extreme form of density-dependent polyphenism known as phase change. Local population density induces the expression of graded changes in a suite of traits that Corresponding author. School of Biological Sciences, The University of Sydney, Heydon-Laurence Building A08, NSW 2006, Australia. Tel.: +61 2 93515633; fax: +61 2 93514119. E-mail address: [email protected] (S.J. Simpson).
0022-1910/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2007.05.011
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include colouration, morphometry, anatomy, egg mass, food selection, nutritional physiology, reproductive physiology, metabolism, neurophysiology, endocrine physiology, molecular biology, immune responses, longevity and pheromone production (Pener, 1991; Pener and Yerushalmi, 1998; Simpson et al., 1999, 2005; Tanaka, 2001, 2006; Ferenz and Seidelmann, 2003; Kang et al., 2004; Hassanali et al., 2005; De Loof et al., 2006; Simpson and Sword, 2007). The extreme forms are termed solitaria (the solitarious phase) and gregaria (the gregarious phase). Uvarov (1966, p. 332) argued that the term ‘solitarious’
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should be used instead of the ambiguous ‘solitary’; we apply this convention here. Behaviour is the phase trait which responds most rapidly to a change in population density, and provides positive feedback which couples other less labile traits and drives the process of phase change at a population level (Simpson et al., 1999; Simpson and Sword, 2007). Gregarious locust behaviour differs from that of solitarious counterparts; most notably, gregarious individuals (1) are attracted to rather than repelled by other locusts, (2) exhibit increased locomotor activity, and (3) demonstrate a tendency to form marching bands as nymphs and day-flying swarms as adults (Simpson et al., 1999). Phase state not only changes within an individual’s lifetime but also transmits epigenetically between generations. Present understanding of transgenerational phase control stems from early studies (Faure, 1932; Gunn and Hunter-Jones, 1952; Hunter-Jones, 1958) in which hatchling colouration was shown to depend on parental rearing density; crowded parents produce darker hatchlings characteristic of the gregarious phase, while solitarious locusts produce light green coloured hatchlings (Uvarov, 1966). These observations have since been extended: many offspring features, including morphometry, behaviour, hatchling mass and development time, are related to parental rearing density (Pener and Yerushalmi, 1998; Simpson et al., 1999; Rahman et al., 2002). At least 45 independent experiments and associated controls have investigated which aspects of parental and egg treatments affect hatchling behaviour and colouration. These experiments are summarised in Table 1, which deals with treatments applied to solitary-reared mothers and their eggs, and Table 2, which concerns crowd-reared mothers and their progeny. We will first pre´cis the phenomenon of transgenerational accumulation of phase state by reference to the experiments as numbered in Tables 1 and 2. We next consider evidence for the nature of agent responsible for the phenomenon.
2. Transmitting gregarious characteristics across generations The extent to which solitary-reared mothers produce hatchlings that behave gregariously depends upon the recency of crowding relative to oviposition (e.g., Table 1, exp. 9, Bouaı¨ chi et al., 1995). The female need not experience crowding directly: mating with a crowd-reared male results in a majority of behaviourally gregarized hatchlings (exp. 8, Islam et al., 1994a). Such effects translate into the field situation, as shown by the observation that hatchling behavioural gregarization could be induced by food plants distributed in a clumped rather than a dispersed manner when solitary-reared adults were kept in field enclosures (exp. 16, Despland and Simpson, 2000). Clumped resource distribution at small spatial scales encourages congregation and subsequent gregarization of
solitarious locusts (Collett et al., 1998; Despland et al., 2000). Behavioural phase state correlates with colouration; treatments that induce behavioural gregarization tend to produce darker-coloured hatchlings. However, the correlation is relatively weak, with colouration only explaining 10% of the variance in behaviour (Islam et al. 1994a). The experiments summarised in Table 1 illustrate an overwhelming trend: behaviour precedes colouration as an indicator of gregarious phase transformation. In only one case of the 23 experiments surveyed in Table 1 did colour change appear to precede behavioural gregarization—the case (exp. 7) in which solitary-reared adults laid in tubes containing greater than three recently laid gregarious egg pods (McCaffery et al., 1998). 3. Transmitting solitarious characteristics across generations The effect of parental population density on hatchling phase state occurs in both gregarizing and solitarizing contexts. Whereas crowding solitary-reared parents leads to development of gregarious features in hatchlings, isolating crowd-reared adults results in only partial solitarization of hatchlings. However, the effect on hatchling phase state of a short period of isolation in gregarious females does not last as long as does a period of crowding in solitary-reared females (Table 1, exp. 9, Bouaı¨ chi et al., 1995). Hence, solitarization of hatchlings was partially induced when crowd-reared females were isolated at the time of oviposition (Table 2, exp. 38), but not if females or their mates were separated from the crowd at the time of mating and then returned to the crowd (exp. 26, Islam et al., 1994b). Rather than behaviour being more labile than colouration, as is the case for acquisition of gregarious characters, gregarious behaviour and colouration are ‘lost’ (i.e., behavioural and pigmentary solitarization occurs) at roughly equal rates. In only three cases of the 11 for which both behaviour and colouration were measured did partial colour change precede behavioural change (exps. 34 and 35) or vice versa (exp. 45). In exp. 45 (Ha¨gele et al., 2000), there was a clear disconnection between colour and behaviour, further indicating that, although these traits are correlated, they do not necessarily share the same underlying mechanisms. In that experiment, the accessory glands were ligatured in gregarious females; hatchlings emerged behaviourally solitarized but black rather than green in colour. 4. The nature of the maternally produced gregarizing agent A series of experiments indicates that gregarizing activity is found in the foam deposited with the eggs during oviposition (exps. 6, 13, 22 and 32). The active material is present in aqueous extracts of egg foam and degrades rapidly, losing its effect if stored for more than 24 h.
Experiments are sorted approximately by increasing magnitude of the gregarizing effect on hatchlings.
Table 1 Effects of various treatments of solitary-reared mothers and their eggs on hatchling colouration and behaviour
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Experiments are sorted approximately by increasing magnitude of the solitarizing effect on hatchlings.
Table 2 Effects of various treatments of crowd-reared mothers and their eggs on hatchling colouration and behaviour
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Additionally, eggs from solitary-reared females only remain sensitive to application of the material during the first day after laying, after which they become refractory (exp. 22, McCaffery et al., 1998). Activity resides in the filtrate after aqueous foam extracts are passed through a 3 kD filter, and heat treatment causes substantial loss of activity (exp. 22, McCaffery et al., 1998). When eggs of crowd-reared females were separated from the pod and incubated individually, with (exp. 42 and 44) or without (exps. 39, 41 and 43) saline washing, a successively greater proportion of green-coloured hatchlings was produced as the time between oviposition and egg separation decreased (McCaffery et al., 1998). This solitarizing effect of egg separation was lost once the interval exceeded 10–24 h (McCaffery et al., 1998), which is consistent with treatments in which hatchling gregarization occurred when aqueous extracts of fresh gregarious egg foam were applied to newly solitary-laid eggs. It was noted that early separation of eggs appeared to be less effective at solitarizing hatchlings when the eggs were not freshly ovulated, implying that eggs could become refractory (i.e., committed to gregarious development) if held within the oviducts (McCaffery et al., 1998; Ha¨gele et al., 2000). We return to this point below. Behavioural gregarization can be reinstated if earlyseparated eggs from crowd-reared parents are treated with aqueous extracts of female accessory glands (exp 33), whereas ligaturing of the accessory glands results in production of behaviourally solitarized hatchlings from eggs laid by crowd-reared females (exp. 45, Ha¨gele et al., 2000). Such hatchlings remained black, however, indicating either that colour determination is under separate control from behaviour or there is an alternative source of gregarizing material within the reproductive tract. In this regard, it is noteworthy that the walls of the oviduct possess glandular cells that appear identical to those of the accessory glands (Szopa, 1981; Ha¨gele et al., 2000). Results from Islam (1997), McCaffery et al. (1998) and Ha¨gele et al. (2000) indicate that gregarizing activity resides in aqueous fractions of egg foam and accessory glands from crowd-reared females. As can be seen in Table 1 and Fig. 1, the capacity of egg foam extracts from crowd-reared females to induce dark colouration in freshly laid eggs from solitary-reared females relates strongly to the polarity of the solvent: hexane, chloroform and acetone extracts had no effect; ethanol had a minor effect; and saline extracts induced the greatest degree of darkening (albeit not full black colouration). Behavioural gregarizing activity was, furthermore, found to be present in the filtrate after aqueous foam extracts were passed through a 3 kD filter. Heat treatment at 100 1C for 10 min caused partial inactivation (McCaffery et al., 1998). Recently, Tanaka and Maeno (2006) did not find that hatchlings became green upon early separation of eggs from crowd-reared females (exps. 28 and 29). Eggs from freshly laid gregarious pods were separated, left unwashed or washed with saline then distilled water, and incubated
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singly. The vast majority of resulting hatchlings were black. These authors concluded that hatchling colouration is committed prior to oviposition and questioned the presence of the maternal gregarizing agent in egg foam. There are two plausible explanations for Tanaka and Maeno’s results. The first relates to the high egg mortality reported (Fig. 2 in Tanaka and Maeno, 2006). In previous work (e.g., Ha¨gele et al., 2000), over 80% of separated eggs survived to hatching; in contrast, Tanaka and Maeno report survival of 15% of separated and washed eggs, while un-separated, control eggs suffered 65% mortality, implying problems with infection or some other stressor. Given that dark hatchlings are larger and more robust than green ones (Hunter-Jones, 1958; Tanaka and Maeno, 2006), it is likely that eggs destined to become green hatchlings suffered disproportionate mortality, allowing remaining black hatchlings to predominate. It has been shown, albeit not for young nymphs, that dark colour forms of locusts and caterpillars have higher resistance to immune challenges, in part because of the involvement of phenyloxidases in both immunity and melanization (Wilson et al., 2001, 2002). A second possible reason for the lack of effect of early egg separation concerns the way in which eggs were collected. Tanaka and Maeno (2006) provided crowdreared females with oviposition medium for 7 h each day. This procedure is commonly used, since depriving insects of an egg-laying site helps synchronise laying and hence facilitates egg pod collection. However, as was discussed by McCaffery et al. (1998, p. 361), who also reported a degree of inconsistency in the solitarizing effect of egg separation, the failure of early egg separation to solitarize hatchlings in some experiments ‘may lie in the degree of exposure of the eggs in the oviducts to the gregarizing factor before oviposition. Possible changes in the length of time that eggs remain in the oviducts before oviposition could affect their degree of prior commitment to the gregarious phase and may need to be controlled in future experiments’. Depriving females of oviposition sites results in less behavioural solitarization of hatchlings than separation of recently ovulated, freshly laid eggs from undeprived crowd-reared females (Ha¨gele et al., 2000) [note that Ha¨gele et al. (2000) scored hatchling colouration only for the accessory gland ligation experiment and not for egg washing experiments as reported by Tanaka and Maeno (2006, p. 1060)]. The lack of solitarization in hatchlings from ‘withheld’ eggs, despite washing, is consistent with observations that (a) the gregarizing agent is released into the reproductive tract from the accessory glands and possibly also the epithelial lining of the oviducts (see above) (Ha¨gele et al., 2000), and (b) eggs only remain responsive to external chemical cues for a brief period, after which they commit to a particular developmental trajectory (McCaffery et al., 1998). While it seems likely that Tanaka and Maeno’s results may have resulted either from very high egg mortality or delayed oviposition, they suggest another important
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Fig. 1. (A) Hatchling colouration resulting from treatment of eggs laid by solitary-reared females with gregarious egg foam extracted by various solvents. Data are from Islam (1997) and McCaffery et al. (1998). Colour scale: 1: uniform green, no black markings; 2: ground colour green with some black markings (o30% of body surface); 3: ground colour green or olive with extensive black markings (30–60% of body surface); 4: black markings 80% of the body surface; 5: heavy black markings (480% of body surface). Hexane, n ¼ 21; chloroform, n ¼ 5; acetone, n ¼ 53; ethanol, n ¼ 47; saline, n ¼ 45. (B) No fully black hatchlings were produced, but dark hatchlings with colour score 3 or greater are produced (solid line) by eggs treated with foam extracts made with high, but not low, polarity solvents. Partition coefficients (dotted line) calculated by regression techniques (Leo and Hansch, 1971; Nys and Rekker, 1973; Valvani et al., 1981) show that even the most polar (James, 1986) of ketones reported by Malual et al. (2001) has a strong (greater than 200fold) preference for organic solvents over water. Solvent dielectric constants (Lane and Saxon, 1952; Lide, 2006) indicate relative polarity.
possibility: genetic and/or environmental (culturing) differences between laboratory strains. A clear example of such strain differences is that between rates of behavioural gregarization measured using the same assay system in solitary-reared insects from the Leuven versus Oxford cultures (Roessingh and Simpson, 1994; Hoste et al., 2002). Malual et al. (2001) confirmed McCaffery et al.’s (1998) finding that egg pods from gregarious females contain a behaviourally gregarizing agent. Oviposition tubes filled with moistened sand were offered to crowd-reared females for 24 h. The egg pods were removed and sand was sifted, allowed to dry overnight and then remoistened. When eggs
from solitary-reared females were incubated in this contaminated sand, hatchlings emerged with an enhanced tendency to form aggregations (a feature of behavioural gregarization). The time between the laying of eggs by crowd-reared females and exposure of solitary-reared eggs to gregarizing compounds was 12–36 h. These data are consistent with results of McCaffery et al. (1998, Figs. 1 and 2), who reported partial hatchling gregarization (colour more pronounced than behaviour) when solitaryreared females oviposited into sand containing multiple pods from crowd-reared females. This gregarizing effect was abolished if the contaminated sand was first incubated
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for 24 h (McCaffery et al., 1998, Fig. 3)—as expected from the observation that the gregarizing agent lost bioactivity within 24 h of production (McCaffery et al., 1998, Fig. 11). Malual et al. (2001) suggested that C-8 unsaturated ketones are responsible for the gregarizing effect of contaminated sand into which crowd-reared females had oviposited previously. This inference was based on three observations. First, hatchlings showed no increased tendency to aggregate if incubated in contaminated sand that had been washed with methanol, acetone and dichloromethane and then dried for 24 h before being remoistened and used to incubate eggs from solitary-reared females (Malual et al., 2001). This treatment would have washed out C-8 unsaturated ketones, but methanol extraction will at least partially remove low-molecular weight polar compounds (see Fig. 1; dielectric constant for methanol is 33). The solvent washing and drying process added a further 24 h to the 12–36 h pretreatment period, by which time polar gregarizing compounds would have degraded (McCaffery et al., 1998, Fig. 11). Second, contaminated sand did not gregarize solitary-laid hatchlings if flushed for 24 h with gaseous nitrogen. Again, the further 24-h period would have resulted in the degradation of the gregarizing compound described by McCaffery et al. (1998). Third, chemical analysis of volatiles emanating from contaminated sand and crushed crowd-laid eggs indicated the presence of C-8 unsaturated ketones, which disappeared after nitrogen flushing. These compounds were detected in the accessory glands of gravid crowd-reared females, in accordance with the conclusion of Ha¨gele et al. (2000) that accessory gland extracts have powerful gregarizing effects. However, given the limited predicted aqueous solubility of the unsaturated C8 ketones (Fig. 1), it is hard to explain how ketones could account for highest levels of bioactivity being found in aqueous and not organic extracts of egg foam (Islam, 1997; McCaffery et al., 1998). Malual et al. (2001) did not report directly testing the effects on hatchling behaviour of applying C8-unsaturated ketones, either to the eggs or to the sand in which they were incubated. Tawfik et al. (1999) found that eggs laid by gregarious females have substantially higher total ecdysteroid content than those of solitarious females. Ha¨gele et al. (2004) investigated the possibility that ecdysteroids might be involved in the maternal transmission of phase state to developing embryos. Total ecdysteroid content was measured in eggs laid by solitary- and crowd-reared females, and of solitary-reared females that had been crowded for 2–48 h, sufficient time to induce development of gregarious behaviour in hatchlings (Islam et al., 1994b), immediately before laying their eggs. Similar differences to those reported by Tawfik et al. (1999) were found between eggs laid by solitary- and crowd-reared females. However, elevated ecdysteroid levels were not stimulated by crowding solitary-reared females immediately prior to oviposition: total ecdysteroid contents of eggs were indistinguishable from solitary-reared females that had not been crowded.
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Hence, ecdysteroids were not responsible for development of gregarious behavioural traits, either directly or as mediators of the action of the maternally produced gregarizing agent. Rahman et al. (2003; see also De Loof et al., 2006) reported that a 6.08-kD peptide that was found to occur at higher levels in the haemolymph of gregarious than solitarious adults was also present in the freshly laid eggs of crowd-reared females at higher concentrations than in solitary-reared females. Clearly the peptide is not the same as McCaffery et al.’s small molecular weight, aqueous gregarizing agent, nor Malual et al.’s (2001) unsaturated C8 ketones, but it could conceivably play a role in determining hatchling phase state. 5. Conclusion The epigenetic transfer of phase state across generations in locusts is clearly a rich phenomenon that has begun to yield to integrated experiments involving large numbers of treatments and their controls. A primary conclusion arising from the present review is that, in solitary-reared insects, transgenerational behavioural changes are more easily triggered than colouration changes. Interestingly, this trend is not apparent for crowd-reared insects; relative to solitary-reared mothers, they more persistently pass their complete phase state to their offspring. Hence, as is made explicit by comparison of analogous treatments in Tables 1 and 2, transgenerational solitarization is more difficult to evoke than gregarization. Such a hysteresis effect has also been shown to exist within an individual’s lifetime and has important population-level consequences (see Simpson et al., 1999). The balance of evidence indicates that the maternal gregarizing influence comes from small molecular weight, aqueous compound(s) released from the reproductive accessory glands and perhaps also from what appears to be identical glandular tissue lining the oviduct. Exposure to this material soon after ovulation, in the oviduct fluid and/ or in the egg foam after oviposition, results in the graded development of gregarious behaviour and colouration in the resulting hatchlings. The chemical identity of this material is yet to be established. Progress has been made, however, and this will be the subject of a forthcoming publication (Miller et al., in preparation). Finally, it is extremely encouraging that recent advances in genomics, proteomics and bioinformatics (see recent review by De Loof et al., 2006; also Kang et al., 2004) offer abundant new opportunities for further exploring the nature and mechanisms of the transgenerational accumulation of phase state in locusts. Acknowledgements This review was written while S.J.S. was in receipt of an Australian Research Council Federation Fellowship.
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G.A.M. was supported by an Oxford Clarendon Fellowship. References Bouaı¨ chi, A., Roessingh, P., Simpson, S.J., 1995. An analysis of the behavioural effects of crowding and re-isolation on solitary-reared adult desert locusts (Schistocerca gregaria) and their offspring. Physiological Entomology 20, 199–208. Collett, M., Despland, E., Simpson, S.J., Krakauer, D.C., 1998. Spatial scales of desert locust gregarization. Proceedings of the National Academy of Sciences of the United States of America 95, 13052–13055. De Loof, A., Claeys, I., Simonet, G., Verleyen, P., Vandersmissen, T., Sas, F., Huybrechts, J., 2006. Molecular markers of phase transition in locusts. Insect Science 13, 3–12. Despland, E., Simpson, S.J., 2000. Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust. Physiological Entomology 25, 74–81. Despland, E., Collett, M., Simpson, S.J., 2000. Small-scale processes in desert locust swarm formation: how vegetation patterns influence gregarization. Oikos 88, 652–662. Faure, J.C., 1932. The phases of locusts in South Africa. Bulletin of Entomological Research 23, 293–405. Ferenz, H.-J., Seidelmann, K., 2003. Pheromones in relation to aggregation and reproduction in desert locusts. Physiological Entomology 28, 11–18. Gunn, D.L., Hunter-Jones, P., 1952. Laboratory experiments on phase differences in locusts. Anti-Locust Bulletin 12, 1–29. Ha¨gele, B.F., Oag, V., Bouaı¨ chi, A., McCaffery, A.R., Simpson, S.J., 2000. The role of female accessory glands in maternal inheritance of phase in the desert locust Schistocerca gregaria. Journal of Insect Physiology 46, 275–280. Ha¨gele, B.F., Wang, F-H., Sehnal, F., Simpson, S.J., 2004. Effects of crowding, isolation, and transfer from isolation to crowding on total ecdysteroid content of eggs in Schistocerca gregaria. Journal of Insect Physiology 50, 621–628. Hassanali, A., Njagi, P.G.N., Bashir, M.O., 2005. Chemical ecology of locusts and related acridids. Annual Review of Entomology 50, 223–245. Hoste, B., Simpson, S.J., Tanaka, S., Zhu, D.-H., De Loof, A., Breuer, M., 2002. Effects of [His7]-corazonin on the phase state of isolatedreared (solitarious) desert locusts, Schistocerca gregaria. Journal of Insect Physiology 48, 981–990. Hunter-Jones, P., 1958. Laboratory studies on the inheritance of phase characters in locusts. Anti-Locust Bulletin 29, 1–32. Islam, M.S., 1997. A preliminary report on the biochemical properties of a maternally-produced gregarizing factor in the desert locust, Schistocerca gregaria (Forskal). Journal of the Asiatic Society of Bangladesh. Science 23, 111–122. Islam, M.S., Roessingh, P., Simpson, S.J., McCaffery, A.R., 1994a. Parental effects on the behaviour and colouration of nymphs of the desert locust Schistocerca gregaria. Journal of Insect Physiology 40, 173–181. Islam, M.S., Roessingh, P., Simpson, S.J., McCaffery, A.R., 1994b. Effects of population density experienced by parents during mating and oviposition on the phase of hatchling desert locusts, Schistocerca gregaria. Proceedings of the Royal Society of London, B 257, 93–98. James, K.C., 1986. Solubility and Related Properties. Marcel Dekker, Inc., New York and Basel. Kang, L., Chen, X.Y., Zhou, Y., Liu, B.W., Zheng, W., Li, R.Q., Wang, J., Yu, J., 2004. The analysis of large-scale gene expression correlated to the phase changes of the migratory locust. Proceedings of the National Academy of Sciences of the United States of America 101, 17611–17615. Lane, J., Saxon, J., 1952. Dielectric dispersion in pure polar liquids at very high frequencies, III. The effect of electrolytes in solution. Proceedings of the Royal Society of London, A 213, 531–545.
Leo, A., Hansch, C., 1971. Linear free-energy relationships between partitioning solvent systems. Journal of Organic Chemistry 36, 1539. Lide, D.R. (Ed.), 2006. CRC Handbook of Chemistry and Physics. CRC Press, Boca Raton, FL. Malual, A.G., Hassanali, A., Torto, B., Assad, Y.O.H., Njagi, P.G.N., 2001. The nature of the gregarizing signal responsible for maternal transfer of phase to the offspring in the desert locust Schistocerca gregaria. Journal of Chemical Ecology 27, 1423–1435. McCaffery, A.R., Simpson, S.J., Islam, M.S., Roessingh, P., 1998. A gregarizing factor present in the egg pod foam of the desert locust Schistocerca gregaria. Journal of Experimental Biology 201, 347–363. Nys, G.G., Rekker, R.F., 1973. Statistical-analysis of a series of partitioncoefficients with special reference to predictability of folding of drug molecules—introduction of hydrophobic fragmental constants (F-values). Chimica Therapeutica 8, 521–535. Pener, M.P., 1991. Locust phase polymorphism and its endocrine relations. Advances in Insect Physiology 23, 1–79. Pener, M.P., Yerushalmi, Y., 1998. The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44, 365–377. Rahman, M.M., Hoste, B., De Loof, A., Breuer, M., 2002. Developmental effect of egg pod foam in the desert locust Schistocerca gregaria (Caelifera: Acrididae). Entomologia Generalis 26, 161–172. Rahman, M.M., Baggerman, G., Begum, M., De Loof, A., Breuer, M., 2003. Purification, isolation and search for possible functions of a phase-related 6080-Da peptide from the haemolymph of the desert locust, Schistocerca gregaria. Physiological Entomology 28, 39–45. Roessingh, P., Simpson, S.J., 1994. The time-course of behavioural phase change in nymphs of the desert locust, Schistocerca gregaria. Physiological Entomology 19, 191–197. Simpson, S.J., Sword, G.A., 2007. Phase polyphenism in locusts: mechanisms, population consequences, adaptive significance and evolution. In: Whitman, D., Ananthakrishnan, T.N. (Eds.), Phenotypic Plasticity in Insects: Mechanisms and Consequences. Science Publishers, Inc., Plymouth, UK, in press. Simpson, S.J., McCaffery, A.R., Ha¨gele, B.F., 1999. A behavioural analysis of phase change in the desert locust. Biological Reviews of the Cambridge Philosophical Society 74, 461–480. Simpson, S.J., Sword, G.A., De Loof, A., 2005. Advances, controversies and consensus in locust phase polyphenism research. Journal of Orthoptera Research 14, 213–222. Szopa, T.M., 1981. The role of the accessory reproductive glands and genital ducts in egg pod formation in female Schistocerca gregaria. Journal of Insect Physiology 27, 23–29. Tanaka, S., 2001. Endocrine nechanisms controlling body-color polymorphism in locusts. Archives of Insect Biochemistry and Physiology 47, 139–149. Tanaka, S., 2006. Corazonin and locust phase polyphenism. Applied Entomology and Zoology 41, 179–193. Tanaka, S., Maeno, K., 2006. Phase-related body-color polyphenism in hatchlings of the desert locust, Schistocerca gregaria: re-examination of the maternal and crowding effects. Journal of Insect Physiology 52, 1054–1061. Tawfik, A.I., Verdova, A., Sehnal, F., 1999. Ecdysteroids during ovarian development and embryogenesis in solitary and gregarious Schistocerca gregaria. Archives of Insect Biochemistry and Physiology 41, 134–143. Uvarov, B., 1966. Grasshoppers and Locusts: A Handbook of General Acridology, vol. 1. Cambridge University Press, London. Valvani, S.C., Yalkowsky, S.H., Roseman, T.J., 1981. Solubility and partitioning. 4. Aqueous solubility and octanol-water partitioncoefficients of liquid non-electrolytes. Journal of Pharmaceutical Sciences 70, 502–507. Wilson, K., Cotter, S.C., Reeson, A.F., Pell, J.K., 2001. Melanism and disease resistance in insects. Ecology Letters 4, 637–649. Wilson, K., Thomas, M.B., Blanford, S., Doggett, M., Simpson, S.J., Moore, S.L., 2002. Coping with crowds: density-dependent disease resistance in desert locusts. Proceedings of the National Academy of Sciences of the United States of America 99, 5471–5475.
Journal of Insect Physiology 53 (2007) 869–876 www.elsevier.com/locate/jinsphys
Review
Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: A review of current understanding Stephen J. Simpsona,b,, Gabriel A. Millera,b a
School of Biological Sciences, The University of Sydney, Heydon-Laurence Building A08, NSW 2006, Australia b Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Received 30 April 2007; received in revised form 21 May 2007; accepted 24 May 2007
Abstract Desert locusts demonstrate pronounced density-dependent polyphenism: a complex suite of traits shifts over the lifetime of an individual in response to crowding or isolation. These changes also accumulate across generations through a maternal effect. Female desert locusts alter the developmental trajectory of their offspring in response to their own experience of crowding. The mother possesses a memory of both the recency and extent of crowding and shifts the phase state of her hatchlings accordingly. Extensive experimental work has shown that offspring behaviour is controlled by a low molecular weight, polar compound (or compounds) released from the mother’s accessory glands. The chemical identity of this agent is not yet known. r 2007 Elsevier Ltd. All rights reserved. Keywords: Schistocerca gregaria; Maternal inheritance; Phase change; Locust; Epigenetic effect
Contents 1. 2. 3. 4. 5.
The maternal control of phase state in the desert locust . . Transmitting gregarious characteristics across generations . Transmitting solitarious characteristics across generations . The nature of the maternally produced gregarizing agent . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. The maternal control of phase state in the desert locust The desert locust, Schistocerca gregaria, demonstrates an extreme form of density-dependent polyphenism known as phase change. Local population density induces the expression of graded changes in a suite of traits that Corresponding author. School of Biological Sciences, The University of Sydney, Heydon-Laurence Building A08, NSW 2006, Australia. Tel.: +61 2 93515633; fax: +61 2 93514119. E-mail address: [email protected] (S.J. Simpson).
0022-1910/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2007.05.011
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include colouration, morphometry, anatomy, egg mass, food selection, nutritional physiology, reproductive physiology, metabolism, neurophysiology, endocrine physiology, molecular biology, immune responses, longevity and pheromone production (Pener, 1991; Pener and Yerushalmi, 1998; Simpson et al., 1999, 2005; Tanaka, 2001, 2006; Ferenz and Seidelmann, 2003; Kang et al., 2004; Hassanali et al., 2005; De Loof et al., 2006; Simpson and Sword, 2007). The extreme forms are termed solitaria (the solitarious phase) and gregaria (the gregarious phase). Uvarov (1966, p. 332) argued that the term ‘solitarious’
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should be used instead of the ambiguous ‘solitary’; we apply this convention here. Behaviour is the phase trait which responds most rapidly to a change in population density, and provides positive feedback which couples other less labile traits and drives the process of phase change at a population level (Simpson et al., 1999; Simpson and Sword, 2007). Gregarious locust behaviour differs from that of solitarious counterparts; most notably, gregarious individuals (1) are attracted to rather than repelled by other locusts, (2) exhibit increased locomotor activity, and (3) demonstrate a tendency to form marching bands as nymphs and day-flying swarms as adults (Simpson et al., 1999). Phase state not only changes within an individual’s lifetime but also transmits epigenetically between generations. Present understanding of transgenerational phase control stems from early studies (Faure, 1932; Gunn and Hunter-Jones, 1952; Hunter-Jones, 1958) in which hatchling colouration was shown to depend on parental rearing density; crowded parents produce darker hatchlings characteristic of the gregarious phase, while solitarious locusts produce light green coloured hatchlings (Uvarov, 1966). These observations have since been extended: many offspring features, including morphometry, behaviour, hatchling mass and development time, are related to parental rearing density (Pener and Yerushalmi, 1998; Simpson et al., 1999; Rahman et al., 2002). At least 45 independent experiments and associated controls have investigated which aspects of parental and egg treatments affect hatchling behaviour and colouration. These experiments are summarised in Table 1, which deals with treatments applied to solitary-reared mothers and their eggs, and Table 2, which concerns crowd-reared mothers and their progeny. We will first pre´cis the phenomenon of transgenerational accumulation of phase state by reference to the experiments as numbered in Tables 1 and 2. We next consider evidence for the nature of agent responsible for the phenomenon.
2. Transmitting gregarious characteristics across generations The extent to which solitary-reared mothers produce hatchlings that behave gregariously depends upon the recency of crowding relative to oviposition (e.g., Table 1, exp. 9, Bouaı¨ chi et al., 1995). The female need not experience crowding directly: mating with a crowd-reared male results in a majority of behaviourally gregarized hatchlings (exp. 8, Islam et al., 1994a). Such effects translate into the field situation, as shown by the observation that hatchling behavioural gregarization could be induced by food plants distributed in a clumped rather than a dispersed manner when solitary-reared adults were kept in field enclosures (exp. 16, Despland and Simpson, 2000). Clumped resource distribution at small spatial scales encourages congregation and subsequent gregarization of
solitarious locusts (Collett et al., 1998; Despland et al., 2000). Behavioural phase state correlates with colouration; treatments that induce behavioural gregarization tend to produce darker-coloured hatchlings. However, the correlation is relatively weak, with colouration only explaining 10% of the variance in behaviour (Islam et al. 1994a). The experiments summarised in Table 1 illustrate an overwhelming trend: behaviour precedes colouration as an indicator of gregarious phase transformation. In only one case of the 23 experiments surveyed in Table 1 did colour change appear to precede behavioural gregarization—the case (exp. 7) in which solitary-reared adults laid in tubes containing greater than three recently laid gregarious egg pods (McCaffery et al., 1998). 3. Transmitting solitarious characteristics across generations The effect of parental population density on hatchling phase state occurs in both gregarizing and solitarizing contexts. Whereas crowding solitary-reared parents leads to development of gregarious features in hatchlings, isolating crowd-reared adults results in only partial solitarization of hatchlings. However, the effect on hatchling phase state of a short period of isolation in gregarious females does not last as long as does a period of crowding in solitary-reared females (Table 1, exp. 9, Bouaı¨ chi et al., 1995). Hence, solitarization of hatchlings was partially induced when crowd-reared females were isolated at the time of oviposition (Table 2, exp. 38), but not if females or their mates were separated from the crowd at the time of mating and then returned to the crowd (exp. 26, Islam et al., 1994b). Rather than behaviour being more labile than colouration, as is the case for acquisition of gregarious characters, gregarious behaviour and colouration are ‘lost’ (i.e., behavioural and pigmentary solitarization occurs) at roughly equal rates. In only three cases of the 11 for which both behaviour and colouration were measured did partial colour change precede behavioural change (exps. 34 and 35) or vice versa (exp. 45). In exp. 45 (Ha¨gele et al., 2000), there was a clear disconnection between colour and behaviour, further indicating that, although these traits are correlated, they do not necessarily share the same underlying mechanisms. In that experiment, the accessory glands were ligatured in gregarious females; hatchlings emerged behaviourally solitarized but black rather than green in colour. 4. The nature of the maternally produced gregarizing agent A series of experiments indicates that gregarizing activity is found in the foam deposited with the eggs during oviposition (exps. 6, 13, 22 and 32). The active material is present in aqueous extracts of egg foam and degrades rapidly, losing its effect if stored for more than 24 h.
Experiments are sorted approximately by increasing magnitude of the gregarizing effect on hatchlings.
Table 1 Effects of various treatments of solitary-reared mothers and their eggs on hatchling colouration and behaviour
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Experiments are sorted approximately by increasing magnitude of the solitarizing effect on hatchlings.
Table 2 Effects of various treatments of crowd-reared mothers and their eggs on hatchling colouration and behaviour
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Additionally, eggs from solitary-reared females only remain sensitive to application of the material during the first day after laying, after which they become refractory (exp. 22, McCaffery et al., 1998). Activity resides in the filtrate after aqueous foam extracts are passed through a 3 kD filter, and heat treatment causes substantial loss of activity (exp. 22, McCaffery et al., 1998). When eggs of crowd-reared females were separated from the pod and incubated individually, with (exp. 42 and 44) or without (exps. 39, 41 and 43) saline washing, a successively greater proportion of green-coloured hatchlings was produced as the time between oviposition and egg separation decreased (McCaffery et al., 1998). This solitarizing effect of egg separation was lost once the interval exceeded 10–24 h (McCaffery et al., 1998), which is consistent with treatments in which hatchling gregarization occurred when aqueous extracts of fresh gregarious egg foam were applied to newly solitary-laid eggs. It was noted that early separation of eggs appeared to be less effective at solitarizing hatchlings when the eggs were not freshly ovulated, implying that eggs could become refractory (i.e., committed to gregarious development) if held within the oviducts (McCaffery et al., 1998; Ha¨gele et al., 2000). We return to this point below. Behavioural gregarization can be reinstated if earlyseparated eggs from crowd-reared parents are treated with aqueous extracts of female accessory glands (exp 33), whereas ligaturing of the accessory glands results in production of behaviourally solitarized hatchlings from eggs laid by crowd-reared females (exp. 45, Ha¨gele et al., 2000). Such hatchlings remained black, however, indicating either that colour determination is under separate control from behaviour or there is an alternative source of gregarizing material within the reproductive tract. In this regard, it is noteworthy that the walls of the oviduct possess glandular cells that appear identical to those of the accessory glands (Szopa, 1981; Ha¨gele et al., 2000). Results from Islam (1997), McCaffery et al. (1998) and Ha¨gele et al. (2000) indicate that gregarizing activity resides in aqueous fractions of egg foam and accessory glands from crowd-reared females. As can be seen in Table 1 and Fig. 1, the capacity of egg foam extracts from crowd-reared females to induce dark colouration in freshly laid eggs from solitary-reared females relates strongly to the polarity of the solvent: hexane, chloroform and acetone extracts had no effect; ethanol had a minor effect; and saline extracts induced the greatest degree of darkening (albeit not full black colouration). Behavioural gregarizing activity was, furthermore, found to be present in the filtrate after aqueous foam extracts were passed through a 3 kD filter. Heat treatment at 100 1C for 10 min caused partial inactivation (McCaffery et al., 1998). Recently, Tanaka and Maeno (2006) did not find that hatchlings became green upon early separation of eggs from crowd-reared females (exps. 28 and 29). Eggs from freshly laid gregarious pods were separated, left unwashed or washed with saline then distilled water, and incubated
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singly. The vast majority of resulting hatchlings were black. These authors concluded that hatchling colouration is committed prior to oviposition and questioned the presence of the maternal gregarizing agent in egg foam. There are two plausible explanations for Tanaka and Maeno’s results. The first relates to the high egg mortality reported (Fig. 2 in Tanaka and Maeno, 2006). In previous work (e.g., Ha¨gele et al., 2000), over 80% of separated eggs survived to hatching; in contrast, Tanaka and Maeno report survival of 15% of separated and washed eggs, while un-separated, control eggs suffered 65% mortality, implying problems with infection or some other stressor. Given that dark hatchlings are larger and more robust than green ones (Hunter-Jones, 1958; Tanaka and Maeno, 2006), it is likely that eggs destined to become green hatchlings suffered disproportionate mortality, allowing remaining black hatchlings to predominate. It has been shown, albeit not for young nymphs, that dark colour forms of locusts and caterpillars have higher resistance to immune challenges, in part because of the involvement of phenyloxidases in both immunity and melanization (Wilson et al., 2001, 2002). A second possible reason for the lack of effect of early egg separation concerns the way in which eggs were collected. Tanaka and Maeno (2006) provided crowdreared females with oviposition medium for 7 h each day. This procedure is commonly used, since depriving insects of an egg-laying site helps synchronise laying and hence facilitates egg pod collection. However, as was discussed by McCaffery et al. (1998, p. 361), who also reported a degree of inconsistency in the solitarizing effect of egg separation, the failure of early egg separation to solitarize hatchlings in some experiments ‘may lie in the degree of exposure of the eggs in the oviducts to the gregarizing factor before oviposition. Possible changes in the length of time that eggs remain in the oviducts before oviposition could affect their degree of prior commitment to the gregarious phase and may need to be controlled in future experiments’. Depriving females of oviposition sites results in less behavioural solitarization of hatchlings than separation of recently ovulated, freshly laid eggs from undeprived crowd-reared females (Ha¨gele et al., 2000) [note that Ha¨gele et al. (2000) scored hatchling colouration only for the accessory gland ligation experiment and not for egg washing experiments as reported by Tanaka and Maeno (2006, p. 1060)]. The lack of solitarization in hatchlings from ‘withheld’ eggs, despite washing, is consistent with observations that (a) the gregarizing agent is released into the reproductive tract from the accessory glands and possibly also the epithelial lining of the oviducts (see above) (Ha¨gele et al., 2000), and (b) eggs only remain responsive to external chemical cues for a brief period, after which they commit to a particular developmental trajectory (McCaffery et al., 1998). While it seems likely that Tanaka and Maeno’s results may have resulted either from very high egg mortality or delayed oviposition, they suggest another important
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Fig. 1. (A) Hatchling colouration resulting from treatment of eggs laid by solitary-reared females with gregarious egg foam extracted by various solvents. Data are from Islam (1997) and McCaffery et al. (1998). Colour scale: 1: uniform green, no black markings; 2: ground colour green with some black markings (o30% of body surface); 3: ground colour green or olive with extensive black markings (30–60% of body surface); 4: black markings 80% of the body surface; 5: heavy black markings (480% of body surface). Hexane, n ¼ 21; chloroform, n ¼ 5; acetone, n ¼ 53; ethanol, n ¼ 47; saline, n ¼ 45. (B) No fully black hatchlings were produced, but dark hatchlings with colour score 3 or greater are produced (solid line) by eggs treated with foam extracts made with high, but not low, polarity solvents. Partition coefficients (dotted line) calculated by regression techniques (Leo and Hansch, 1971; Nys and Rekker, 1973; Valvani et al., 1981) show that even the most polar (James, 1986) of ketones reported by Malual et al. (2001) has a strong (greater than 200fold) preference for organic solvents over water. Solvent dielectric constants (Lane and Saxon, 1952; Lide, 2006) indicate relative polarity.
possibility: genetic and/or environmental (culturing) differences between laboratory strains. A clear example of such strain differences is that between rates of behavioural gregarization measured using the same assay system in solitary-reared insects from the Leuven versus Oxford cultures (Roessingh and Simpson, 1994; Hoste et al., 2002). Malual et al. (2001) confirmed McCaffery et al.’s (1998) finding that egg pods from gregarious females contain a behaviourally gregarizing agent. Oviposition tubes filled with moistened sand were offered to crowd-reared females for 24 h. The egg pods were removed and sand was sifted, allowed to dry overnight and then remoistened. When eggs
from solitary-reared females were incubated in this contaminated sand, hatchlings emerged with an enhanced tendency to form aggregations (a feature of behavioural gregarization). The time between the laying of eggs by crowd-reared females and exposure of solitary-reared eggs to gregarizing compounds was 12–36 h. These data are consistent with results of McCaffery et al. (1998, Figs. 1 and 2), who reported partial hatchling gregarization (colour more pronounced than behaviour) when solitaryreared females oviposited into sand containing multiple pods from crowd-reared females. This gregarizing effect was abolished if the contaminated sand was first incubated
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for 24 h (McCaffery et al., 1998, Fig. 3)—as expected from the observation that the gregarizing agent lost bioactivity within 24 h of production (McCaffery et al., 1998, Fig. 11). Malual et al. (2001) suggested that C-8 unsaturated ketones are responsible for the gregarizing effect of contaminated sand into which crowd-reared females had oviposited previously. This inference was based on three observations. First, hatchlings showed no increased tendency to aggregate if incubated in contaminated sand that had been washed with methanol, acetone and dichloromethane and then dried for 24 h before being remoistened and used to incubate eggs from solitary-reared females (Malual et al., 2001). This treatment would have washed out C-8 unsaturated ketones, but methanol extraction will at least partially remove low-molecular weight polar compounds (see Fig. 1; dielectric constant for methanol is 33). The solvent washing and drying process added a further 24 h to the 12–36 h pretreatment period, by which time polar gregarizing compounds would have degraded (McCaffery et al., 1998, Fig. 11). Second, contaminated sand did not gregarize solitary-laid hatchlings if flushed for 24 h with gaseous nitrogen. Again, the further 24-h period would have resulted in the degradation of the gregarizing compound described by McCaffery et al. (1998). Third, chemical analysis of volatiles emanating from contaminated sand and crushed crowd-laid eggs indicated the presence of C-8 unsaturated ketones, which disappeared after nitrogen flushing. These compounds were detected in the accessory glands of gravid crowd-reared females, in accordance with the conclusion of Ha¨gele et al. (2000) that accessory gland extracts have powerful gregarizing effects. However, given the limited predicted aqueous solubility of the unsaturated C8 ketones (Fig. 1), it is hard to explain how ketones could account for highest levels of bioactivity being found in aqueous and not organic extracts of egg foam (Islam, 1997; McCaffery et al., 1998). Malual et al. (2001) did not report directly testing the effects on hatchling behaviour of applying C8-unsaturated ketones, either to the eggs or to the sand in which they were incubated. Tawfik et al. (1999) found that eggs laid by gregarious females have substantially higher total ecdysteroid content than those of solitarious females. Ha¨gele et al. (2004) investigated the possibility that ecdysteroids might be involved in the maternal transmission of phase state to developing embryos. Total ecdysteroid content was measured in eggs laid by solitary- and crowd-reared females, and of solitary-reared females that had been crowded for 2–48 h, sufficient time to induce development of gregarious behaviour in hatchlings (Islam et al., 1994b), immediately before laying their eggs. Similar differences to those reported by Tawfik et al. (1999) were found between eggs laid by solitary- and crowd-reared females. However, elevated ecdysteroid levels were not stimulated by crowding solitary-reared females immediately prior to oviposition: total ecdysteroid contents of eggs were indistinguishable from solitary-reared females that had not been crowded.
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Hence, ecdysteroids were not responsible for development of gregarious behavioural traits, either directly or as mediators of the action of the maternally produced gregarizing agent. Rahman et al. (2003; see also De Loof et al., 2006) reported that a 6.08-kD peptide that was found to occur at higher levels in the haemolymph of gregarious than solitarious adults was also present in the freshly laid eggs of crowd-reared females at higher concentrations than in solitary-reared females. Clearly the peptide is not the same as McCaffery et al.’s small molecular weight, aqueous gregarizing agent, nor Malual et al.’s (2001) unsaturated C8 ketones, but it could conceivably play a role in determining hatchling phase state. 5. Conclusion The epigenetic transfer of phase state across generations in locusts is clearly a rich phenomenon that has begun to yield to integrated experiments involving large numbers of treatments and their controls. A primary conclusion arising from the present review is that, in solitary-reared insects, transgenerational behavioural changes are more easily triggered than colouration changes. Interestingly, this trend is not apparent for crowd-reared insects; relative to solitary-reared mothers, they more persistently pass their complete phase state to their offspring. Hence, as is made explicit by comparison of analogous treatments in Tables 1 and 2, transgenerational solitarization is more difficult to evoke than gregarization. Such a hysteresis effect has also been shown to exist within an individual’s lifetime and has important population-level consequences (see Simpson et al., 1999). The balance of evidence indicates that the maternal gregarizing influence comes from small molecular weight, aqueous compound(s) released from the reproductive accessory glands and perhaps also from what appears to be identical glandular tissue lining the oviduct. Exposure to this material soon after ovulation, in the oviduct fluid and/ or in the egg foam after oviposition, results in the graded development of gregarious behaviour and colouration in the resulting hatchlings. The chemical identity of this material is yet to be established. Progress has been made, however, and this will be the subject of a forthcoming publication (Miller et al., in preparation). Finally, it is extremely encouraging that recent advances in genomics, proteomics and bioinformatics (see recent review by De Loof et al., 2006; also Kang et al., 2004) offer abundant new opportunities for further exploring the nature and mechanisms of the transgenerational accumulation of phase state in locusts. Acknowledgements This review was written while S.J.S. was in receipt of an Australian Research Council Federation Fellowship.
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