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6-2011 Regulation of Migration in (Walker) in China: A Review Integrating Environmental, Physiological, Hormonal, Genetic, and Molecular Factors Xingfu Jiang Chinese Academy of Agricultural Sciences

Lizhi Luo Chinese Academy of Agricultural Sciences

Lei Zhang Chinese Academy of Agricultural Sciences

Thomas W. Sappington IFoowlalo Swta tthie Usn iaverndsit ay,dd tsaitppioning@ial wasorktates.e adut: http://lib.dr.iastate.edu/ent_pubs Part of the Agriculture Commons, Biology Commons, Comparative and Evolutionary PYhi Hysiou logy Commons, Ecology and Evolutionary Biology Commons, and the Entomology Chommoninese Academs y of Agricultural Sciences The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ ent_pubs/193. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html.

This Article is brought to you for free and open access by the Entomology at Iowa State University Digital Repository. It has been accepted for inclusion in Entomology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Regulation of Migration in Mythimna separata (Walker) in China: A Review Integrating Environmental, Physiological, Hormonal, Genetic, and Molecular Factors

Abstract Each year the Mythimna separate (Walker), undertakes a seasonal, long-distance, multigeneration roundtrip migration between southern and northern China. Despite its regularity, the decision to migrate is facultative, and is controlled by environmental, physiological, hormonal, genetic, and molecular factors. Migrants take off on days 1 or 2 after eclosion, although the preoviposition period lasts ≈7 d. The trade-offs among the competing physiological demands of migration and reproduction are coordinated in M. separata by the “oogenesis-flight syndrome.” Larvae that experience temperatures above or below certain thresholds accompanied by appropriate humidity, short photoperiod, poor nutrition, and moderate density tend to develop into migrants. However, there is a short window of sensitivity within 24 h after adult eclosion when migrants can be induced to switch to reproductive residents if they encounter extreme environmental factors including starvation, low temperature and long photoperiod. Juvenile hormone (JH) titer is low before migration but high titers are associated with termination of migratory behavior and the switch to reproduction. Early release of JH by the corpora allata in environmentally stressed 1-d old adults, otherwise destined by larval conditions to be migrants, switches them to residents. Offspring inherit parental additive genetic effects governing migratory behavior. However, they also retain flexibility in expression of both flight and reproductive life history traits. The neuropeptide, allatotropin, which activates corpora allata to synthesize JH, controls adult flight and reproduction. Future research directions to better understand regulation of migration in this are discussed.

Keywords Mythimna separata, migration, regulation

Disciplines Agriculture | Biology | Comparative and Evolutionary Physiology | Ecology and Evolutionary Biology | Entomology

Comments This article is from Environmental Entomology 40 (2011): 516, doi:10.1603/EN10199.

Rights Works produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted.

This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/ent_pubs/193 Regulation of Migration in Mythimna separata (Walker) in China: A Review Integrating Environmental, Physiological, Hormonal, Genetic, and Molecular Factors Author(s): Xingfu Jiang, Lizhi Luo, Lei Zhang, Thomas W. Sappington, and Yi Hu Source: Environmental Entomology, 40(3):516-533. 2011. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/EN10199 URL: http://www.bioone.org/doi/full/10.1603/EN10199

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. REVIEW Regulation of Migration in Mythimna separata (Walker) in China: A Review Integrating Environmental, Physiological, Hormonal, Genetic, and Molecular Factors

1,2 1,3 1 4 1 XINGFU JIANG, LIZHI LUO, LEI ZHANG, THOMAS W. SAPPINGTON, AND YI HU

Environ. Entomol. 40(3): 516Ð533 (2011); DOI: 10.1603/EN10199 ABSTRACT Each year the Mythimna separate (Walker), undertakes a seasonal, long-distance, multigeneration roundtrip migration between southern and northern China. Despite its regularity, the decision to migrate is facultative, and is controlled by environmental, physiological, hormonal, genetic, and molecular factors. Migrants take off on days 1 or 2 after eclosion, although the preoviposition period lasts Ϸ7 d. The trade-offs among the competing physiological demands of migration and reproduction are coordinated in M. separata by the “oogenesis-ßight syndrome.” Larvae that expe- rience temperatures above or below certain thresholds accompanied by appropriate humidity, short photoperiod, poor nutrition, and moderate density tend to develop into migrants. However, there is a short window of sensitivity within 24 h after adult eclosion when migrants can be induced to switch to reproductive residents if they encounter extreme environmental factors including starvation, low temperature and long photoperiod. Juvenile hormone (JH) titer is low before migration but high titers are associated with termination of migratory behavior and the switch to reproduction. Early release of JH by the corpora allata in environmentally stressed 1-d old adults, otherwise destined by larval conditions to be migrants, switches them to residents. Offspring inherit parental additive genetic effects governing migratory behavior. However, they also retain ßexibility in expression of both ßight and reproductive life history traits. The insect neuropeptide, allatotropin, which activates corpora allata to synthesize JH, controls adult ßight and reproduction. Future research directions to better understand regulation of migration in this species are discussed.

KEY WORDS Mythimna separata, migration, regulation

Insect migration not only is an adaptive behavioral 2001; McNeil et al. 2005; Bolnick and Nosil 2007; Jiang strategy that has evolved independently within most and Luo 2008). The resulting practical and theoretical insect orders among species inhabiting complex and advances have greatly improved our understanding of uncertain environments, but also is a key factor af- insect migration, which is critical to improved man- fecting insect population abundance and agement of migratory pests (Pedgley 1993, DufÞeld levels (Kennedy 1961, 1985; Southwood 1962, 1977; and Steer 2006, Isard et al. 2009, Nagoshi et al. 2009). Johnson 1969; Southwood et al. 1974; Dingle 1972, The phenomenon of insect migration is often asso- 1982, 1985, 1996; Dingle and Drake 2007; Roff and ciated in a shorthand way with a series of classical Fairbairn 2007). The challenge of attaining a deep monikers and descriptive phrases, such as the “oogen- understanding of insect migration has occupied the esisÐßight syndrome” (Johnson 1963, 1969; Rankin et full attention of many entomologists, compelling them al. 1986, 1994), “migratory syndrome” (Dingle 2001, to delve into a variety of research Þelds including 2006), and “migratory cost and its compensation” ecology, physiology, genetics, evolution, and molec- (Rankin & Burchsted 1992, Zera and Denno 1997), ular biology (Johnson 1963; Rankin 1987, 1991; Dingle based on the observation that it is frequently corre- 1991; Jansons et al. 1996; Gatehouse 1997; Bendena et lated with a typical set of coordinated physiological, al. 1997; McNeil and Tobe 2001; Roff and Fairbairn developmental, and behavioral phenomena that evolved to manage Þtness tradeoffs. Though the ter- minology and underlying concepts are widely ac- 1 State Key Laboratory for Biology of Plant and Insect , cepted and conceptually useful in many contexts, the Institute of Plant Protection, Chinese Academy of Agricultural Sci- ences, 2 West Yuanmingyuan Road Haidian District, Beijing, 100193, relationship between ßight and reproduction is often China. quite complex and can differ from species to species 2 Corresponding author, e-mail: [email protected]. more frequently than these descriptors may imply 3 Corresponding author, e-mail: [email protected]. (Greenbank et al. 1980, Rankin et al. 1986, Sappington 4 USDAÐARS Corn & Genetics Research Unit, Ge- netics Laboratory, Iowa State University, Ames, IA 50011. and Showers 1992, Zhao et al. 2009, Jiang et al. 2010). This is an invited review article. Having a thorough understanding of this relationship

0046-225X/11/0516Ð0533$04.00/0 ᭧ 2011 Entomological Society of America June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 517 is critical to predicting inßuxes of a migrant pest spe- what is the nature of physiological and behavioral cies as well as modeling its population dynamics and preparations for pre- and postmigration activity? damage potential before and after migration. These are critical questions, because although oper- In China, insect damage sustained by the most im- ating at the level of the individual, these mechanisms portant agricultural such as , , , result in the striking pattern of seasonal long-distance cotton, and vegetables are largely the consequence of displacement of populations. by migratory species, most notably the My- This review is concerned exclusively with environ- thimna separate (Walker), mental, physiological, hormonal, genetic, and molec- exigua (Hu¨bner), beet webworm Loxostege sticticalis ular control of M. separata migration, based on Þndings (L.), Locusta migratoria manilensis (Meyen), Nilapa- that have emerged from our studies over the last two rvata lugens (Stal), and the Heliothis armigera (Hu¨ b- decades. Many of these studies were published in ner) (Jiang and Luo 1999, Jiang et al. 2009, Huang and Chinese and our purpose here is to synthesize this Zhu 2001, Cheng et al. 2003, Wu and Guo 2005, Wang body of work so that the global community of scien- et al. 2006). M. separata has been extensively studied tists is fully aware of the progress and key discoveries in China, and has emerged as a model migratory spe- that have been made in this model system. Despite its cies (Li et al. 1964, Chen and Bao 1987, Chen et al. importance, it is beyond the scope of this review to 1995). This insect has been a pest on (Pennis- cover the application of this hard-won knowledge to etum spp.) and wheat (Triticum spp.) for thousands of successful mitigation of the destructiveness of this pest years in China (Zou 1956), and today it damages in China through ecological management and popu- wheat, maize, rice, and other crops (Chen and Hu lation forecasting. After reviewing what has been 2000, Wang et al. 2006). From 1970Ð1978, this insect learned about regulation mechanisms, we conclude was responsible for six nationwide economic disasters with a synthetic account of this speciesÕ migration as (National Statistical Bureau of PeopleÕs Republic of a life history trait, and discuss future directions in light China [NSBPRC] 1995). In recent years, it has been of our recent research. It is our hope that this paper controlled well in most areas of South and Central will contribute both to a better understanding of long- China by decreasing the area of host plant cultivation distance migration in insects in particular, and to mi- in South China where it can survive and reproduce gration theory in general. through the winter. Nevertheless, many regions in North China, where it cannot overwinter, are still Environmental Control regularly infested (Jiang 2004, Zhang 2006). Annual long-distance movement of M. separata be- Because insect migration usually represents an impor- tween overwintering sites in southern China and tant behavioral adaptation for spatially tracking and ex- northern temperate zones occurs naturally via multi- ploiting temporary or seasonal habitats (Kennedy 1985, generation roundtrip migration. Migration routes in Rankin and Burchsted 1992), environmental cues asso- eastern China were revealed by an extensive 3-yr ciated with habitat quality can trigger or inhibit the onset mark-release-recapture study (Li et al. 1964; Fig. 1). of migration, including governance of developmental Based on these data, which are supported by many migratory phase changes (Ramenofsky and WingÞeld years of trap data, radar observations, and weather 2007). As in most insects, ambient environmental con- analyses (Chen et al. 1989, 1995), there are at least four ditions such as temperature, humidity, photoperiod, lar- distinct large-scale migration events of M. separata val density, and nutrition directly inßuence biological annually in eastern China. Two involve northward parameters of M. separata such as growth, survival, and displacement in the spring and early summer (Fig. development rates. In this migratory species, however, 1A,B), and two involve southward displacement in they also serve as cues at developmental decision points summer and fall (Fig. 1C,D). In addition, there are for determining alternative migration and reproduction documented long-distance migration events from east life history pathways. to west and vice versa (Fig. 1B,C), but the seasonal Temperature. Escape from high temperatures in dynamics of M. separata movement in western China South China in spring and summer, and from low are not well understood. temperatures in North China in fall and winter, is one The generational segments of the annual roundtrip of the pressures favoring the annual M. separata migration occur at predictable times of the year and roundtrip migration as an adaptive life history strategy involve all but a small portion of the adults emerging (Jiang et al. 2000). Warm temperature has a generally in a location. Despite the predictability of this seasonal positive inßuence on larval growth, development, and pattern of M. separata migration events, the nature of survival, as well as on adult ßight activity and repro- migratory behavior in individuals is clearly facultative, duction (Jiang and Luo 1997, Jiang et al. 1998). How- in that the decision to migrate mainly depends on ever, extreme high temperatures can have the oppo- environmental cues (Zhang et al. 2006, 2008a). There- site effect, and the disadvantages of high temperatures fore, the insect migration research group at the Insti- to adult reproduction are greater than those incurred tute of Plant Protection, Chinese Academy of Agri- by engaging in migratory ßight, favoring an increase in cultural Sciences has taken on the challenge of the tendency to migrate from regions experiencing or systematically elucidating the underlying mechanisms about to experience extreme heat (Jiang et al. 2000; that govern individual M. separata migratory behavior. Fig. 2). Conversely, cold tolerance of this species de- Which environmental cues regulate migration, and termines the northern limit of its overwintering range 518 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3

Fig. 1. The migratory pathway of M. separata populations in China, based on the mark-release-recapture study of Li et al. (1964), showing seasonal, long-distance, multigeneration roundtrip migration. (A) From March to mid-April, most of the overwintering generation adults (south of 0ЊC isotherm in January) migrate northward to the Þrst generation outbreak region (between 33Њ N and 36Њ N), and a few possibly continue migrating northward. (B) From late May to early June, some adults of the next generation in the Þrst generation outbreak region migrate northeastward to the second generation outbreak region north of 39Њ N. Other adults from the same Þrst generation outbreak region migrate westward or south- westward to western China. (C) From mid to late July, most adults emerging in the second generation outbreak region migrate southward to the third generation outbreak region (between 36Њ N and 39Њ N). In addition, adults emerging in northwest China migrate southwestward and northeastward. (D) From late August to mid September, most adults emerging in the third generation outbreak region migrate southward to the Þfth (between 27Њ N and 32Њ N), or Þrst and Þfth generation outbreak regions (south of 8ЊC isotherm in January). in China. This limit is around 33Њ N latitude, where the unless they migrate far enough south where their average temperature in January is Ϸ0ЊC (Li 1961). offspring can survive the winter. Adults emerging north of this isotherm late in the M. separata migration is inßuenced greatly by tem- season cannot contribute to subsequent generations perature in three distinct ways. Rearing temperature June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 519

Fig. 2. Effects of conditions encountered by M. separata larvae (A), or adults (B), on ßight (black bars) and reproduction (white bars). Means with the same lowercase (black bars) or uppercase (white bars) letter within treatment category are not signiÞcantly different (P Ͼ 0.05). Adult ßight test conditions in panel. (A) Temperature (Jiang et al. 2000): unfed, 1-d-old females, unmated, tethered ßight for 20 h at 24 Ϯ 1ЊC, 70% RH. Photoperiod (Cao et al. 1997): 5-d-old moths, possibly mated (from caged male-female pairs), fed with 5% honey-water, tethered ßight for 12Ð24 h at 23 Ϯ 0.5ЊC, 70Ð80% RH. Rearing density (Luo et al. 1995a): unfed, 1-d-old moths, unmated, tethered ßight for 12 h at 20 Ϯ 0.5ЊC, 60% RH. Larval nutrition (Cao et al. 1996): 1-d-old moths, unmated, tethered ßight for 12 h. Adult ßight test conditions in panel. (B) Temperature (Jiang et al. 2003): 3-d-old females, possibly mated (from caged male-female pairs), tethered ßight for 12 h at indicated temperatures and 70Ð85% RH. Relative humidity (Jiang et al. 2003): 3-d-old females, possibly mated (from caged male-female pairs), tethered ßight for 12 h at 22 Ϯ 1ЊC and indicated RH. Adult nutrition during the Þrst 24 h after eclosion (Zhang et al. 2006): Nonstarved moths received 5% honey-water during Þrst 24 h after eclosion. All moths received 5% honey-water after the Þrst 24 h. Bars are means of distances ßown during 14 h of tethered ßight at 24, 48, 72, 96, 120, and 144 h after starvation, at 24 Ϯ 1ЊC, 70% RH. of immature insects, including eggs, larvae, and pupae, fecundity. Migrant M. separata are characterized by a can induce development into either migrant or resi- longer preoviposition period than residents (Han and dent adults (Jiang et al. 1998, 2000). When reared at Gatehouse 1993, Luo et al. 1995a, Jiang et al. 2005). a constant temperature of 27ЊC, unfed newly emerged Similarly, the male preresponse period to female sex moths showed the highest ßight potential, with the pheromone was shortened after cold-stress the Þrst highest incidence of long-ßiers (Fig. 2A). Concomi- day after eclosion. Conversely, cold shock applied tantly, adult reproductive development declines with after the Þrst 24 h did not switch residents into mi- increasing rearing temperature, as evidenced by de- grants. This phenomenon not only provides evidence creased fecundity, mating rate and longevity. With the of an adult sensitive stage, but also implies a secondary rearing temperature further increasing to 30 and 33ЊC, regulatory pathway in adults (Zhang et al. 2008a). This immature development, adult ßight, and reproduction surprising discovery further highlights an abundance were all negatively affected (Fig. 2A), thus providing of life history ßexibility in this species available in the support for the idea that escape from the harmful face of an uncertain environment. effects of high temperature is one of the factors fa- Tethered ßight (Zhang and Li 1985, Jiang et al. voring evolution of migration as a life-history option 2003) and radar (Chen et al. 1989) studies have re- for this species. vealed that temperature also inßuences M. separata Zhang et al. (2008a) demonstrated that cold-stress migration through its effects on timing of moth take- (5ЊC) experienced during the Þrst 24 h after eclosion off, transfer velocity, direction, distance, and altitude. can switch migrants into residents. This switch away In M. separata, most ßight occurs at temperatures from migration was deduced by a reduction in the between 11 and 32ЊC, with an optimum of Ϸ17Ð22ЊC female preoviposition period and increased lifetime and a lower threshold of 8ЊC. Emigrants can take off 520 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3 only on dates when the air temperature at ground level moth ßight performance, and prolonged female pre- near dusk is at least 8Ð10ЊC, providing important in- oviposition and calling periods, but not decreased fe- formation for population dynamics forecasting (Fig. cundity (Fig. 2A) (Han and Gatehouse 1991a, Cao et 2B) (Zhang and Li 1985, Jiang et al. 2003). Moth al. 1997). This kind of photoperiod response is similar transfer velocity, direction and distance also are in- to that of other noctuid migratory species (Delisle and ßuenced by temperature. Moths can ßy at a speed of McNeil 1987, Hill and Gatehouse 1992). However, in 5Ð6 m/s, which translates to a distance of several M. separata, when individuals destined by larval con- hundred kilometers per night when wind speed is ditions to be migrants were challenged by full day below 5 m/s and temperature is appropriate. How- length within 24 h after eclosion, they switched to ever, moth transport is assisted by winds at higher residents as indexed by decreased moth preoviposi- speeds even at lower temperatures (Zhao 1982, Chen tion period and increased lifetime fecundity (Zhang et al. 1989). Furthermore, altitude of migratory ßight 2006). Those challenged on subsequent days were not has been observed over a wide range, from 300 to 1,000 signiÞcantly inßuenced. This provides further evi- m, a consequence of selecting optimum air tempera- dence of an adult sensitive stage associated with sec- ture (Zhao 1982, Chen et al. 1989, Jiang et al. 2003, ondary regulation in this species (Zhang 2006). Zhang 2008). As a consequence, moth migration alti- Larval Density. M. separata larval density inßuences tude differed depending on the temperatures experi- not only immature development, larval diet utiliza- enced during various seasons at different latitudes. tion, and phase change, but also adult ßight and re- Flight altitude was higher during northward migration production (Fig. 2A) (Luo et al. 1993; Luo et al. from spring to summer, and was lower during south- 1995a,b). Larvae reared at moderate densities develop ward migration from summer to autumn, although the into migrants that exhibit a longer female preovipo- moths are still inßuenced by other weather and geo- sition period, stronger ßight potential, moderate pupal graphical factors (Zhao 1982). and adult size, and fewer eggs laid by females (Luo et Relative Humidity. Although relative humidity can al. 1993, 1995a,b). Another source of variation in moth inßuence immature development, adult ßight and re- ßight performance after being reared under different production, it also plays a role in inducing M. separata larval densities is a difference in ßight energy re- migration, usually in combination with temperature sources, especially accumulated glyceride content (Li (Chin et al. 1964a,b, Cao et al. 1995a, Jiang et al. 2003). and Luo 1998). However, the ratio of migrants devel- Maximum ßight performance was observed when rel- oped from larvae developing under different densities ative humidity was Ϸ75%, combined with appropriate does not increase indeÞnitely with density, but instead temperatures of 18Ð26ЊC (Fig. 2B). Poorer ßight per- peaks at medium larval density (Luo et al. 1995a). At formance was observed with humidity outside these high larval densities, larval survival, adult ßight, and ranges. The combined negative effects of temperature reproductive capacity were also negatively affected and humidity on ßight performance vary with age and (Luo et al. 1993, Luo et al. 1995a). Thus, migrants in sex. In general, young moths are less negatively af- M. separata possibly appear in Þelds when larval den- fected than old moths by high temperature combined sity reaches a threshold of moderate rather than se- with low humidity. Females are less negatively af- vere crowding, which implies that habitat deteriora- fected by high temperature than males, while males tion is not extreme at the onset of migration. This high are less negatively affected by lower humidity (Jiang sensitivity to larval density for migrant induction sug- et al. 2003). gests that most adults emerging from a larval outbreak A mechanism underlying the different combined generation are likely to emigrate. Thus, regulation of inßuences of temperature and relative humidity on migration by larval density in this species is different adult ßight performance is consequent variation in from that in Spodoptera frugiperda (J.E. ßight energy consumption and utilization. Moths Smith) and African armyworm S. exempta (Walker) ßown under suitable temperatures of 18Ð23ЊC and that are induced to migrate by low and high larval Ϸ75% RH consumed less energy substrate per unit densities, respectively (Parker and Gatehouse 1985, distance than under conditions outside these values. Ferguson et al. 1997). These Þndings provide a conceptual basis for energy Nutrition. In M. separata, supplementary nutrition utilization efÞciency as a determinant of migratory in the form of nectar consumed during the adult stage ßight performance (Cai et al. 2002). is necessary for ßight and reproduction, and adequate Photoperiod. Photoperiod is an important environ- nutrition after eclosion is necessary for successful mi- mental cue that can induce a tendency to migrate in gration (Li 1961, Li et al. 1987, Wang et al. 2006). M. separata. In Eastern China, photoperiodic changes Larval diet also signiÞcantly inßuences immature from spring to winter provide dependable environ- growth and development, as well as adult ßight and mental cues that help regulate migration. The use of reproduction (Qin 1964, Qin et al. 1964, Guo and Liu photoperiod also illustrates that M. separata has 1964, Cao et al. 1996, Wang and Zhang 2001). Inter- evolved as a migratory species to adapt to a seasonal estingly, larval diet and adult supplementary nutrition environment that changes predictably (Cao et al. play a substantially different, even contrary role in 1997). Laboratory experiments indicated that both inducing migration in this species. Periodic starvation short photoperiod (LϽ12 h) and gradually decreasing during the larval stage can signiÞcantly increase the photoperiod (L16:D83L12:D12) can signiÞcantly in- tendency of adults to migrate and increases the ratio duce M. separata migration, as evidenced by improved of migrants. Larvae that were starved for 3, 6, and 9 h June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 521 per day after hatching, emerged as adults that dis- ductive status and the expression of migratory behav- played signiÞcantly decreased fecundity (except ior are part of a selective milieu that gives rise to an when larvae starved for 6 h per day), longer preovi- adaptive suite of characters comprising a larger mi- posion periods, and higher average ßight performance gration syndrome or life history syndrome for the (although there were no signiÞcant differences in species (Rankin and Burchsted 1992, Min et al. 2004, ßight distance compared with the control) (Fig. 2A) Dingle and Drake 2007, Roff and Fairbairn 2007, (Cao et al. 1996). As in the case with cold-shock and Ronce 2007). The life history syndrome of a migratory photoperiod (Zhang et al. 2006, 2008a), starvation of species may or may not include a physiological mech- adults within 24 h after adult eclosion switches mi- anism coordinating reproduction and migration in a grants into residents, as evidenced by decreased ßight way that manifests as the classical oogenesis-ßight potential, degenerating ßight muscle, accelerated fe- syndrome (Rankin et al. 1986, Sappington and Show- male ovarian development, and increased fecundity, ers 1992, McNeil et al. 1995, Zhao et al. 2009, Jiang et while starvation at other adult ages has no such effect al. 2010). (Zhang et al. 2008a). This pattern provides additional To illuminate the relationship between M. separata proof of a sensitive adult stage under secondary reg- adult ßight and reproduction and its underlying phys- ulation. iological control, we have investigated the differences in mating status, ovarian development, moth age, and development of the ßight apparatus in moths before Physiological Control and after migration. Although insect migration is a life history trait of Mating Status and Ovarian Development. It is clear adaptive value with important implications for popu- that before migration most female M. separata exhibit lation maintenance and evolution, it is a costly behav- little or no ovarian development and are seldom ior that may require tradeoffs in risks and resource mated, while after migration most females have ma- allocation (Rankin and Burchsted 1992, Crowley and ture ovaries and high mating frequency. During the McLetchie 2002, Kokko and Lo´pez-Sepulcre 2006, second northward migration event (Fig. 1B), that is, Roff and Fairbairn 2007, Ronce 2007). Lifetime re- from late May to early June, in the Þrst generation productive output of females may suffer from diver- outbreak region of Ganyu county (122.25ЊE, 34.50ЊN), sion of metabolic resources needed for ovarian devel- Jiangsu province, most females showed this pattern opment (oogenesis) to construction of the ßight based on comparisons between emigrant and immi- apparatus, particularly ßight muscle protein (Wheeler grant populations in the Þeld (Jiang and Luo 2005). 1996). Moreover, long-distance migratory ßight usu- The average basal ovarium width, length, and wet ally is fueled by mobilized lipid reserves (Van Handel weight, as well as mating rate and mating frequency 1974, Teo et al. 1987, Sappington et al. 1995, Hauner- were signiÞcantly lower than those collected at the land 1997, Candy et al. 1997) and the necessary energy terminus of migration (Table 1). Emigrant males also consumption is costly (Rankin and Burchsted 1992, have little response to sex pheromone, while this re- Wheeler 1996, Canavoso et al. 2001). The potential sponse was stronger in the immigrant populations costs of migration may be manifested by decreased (Han et al. 1990; Table 1). However, during migration, lifetime reproductive potential resulting from a pro- female mating status and ovarian development are longed preoviposition period, which often represents debatable. Wang and Zhang (2001) found that female a substantial proportion of adult life span, as well as by copulation did not occur during migratory ßight, and decreased longevity. Such costs are particularly evi- ovarian development was suspended based on dissec- dent in insects with wing dimorphism (Dingle and tions. Mating and ovarium development initiated Arora 1973, Walters and Dixon 1983, Roff 1984, Zera quickly after entering the calling period, and most 1984, Zera and Mole 1994, Roff and Fairbairn 2007). females were sexually mature within 20 h. However, Whether such tradeoffs between migration and re- recent research demonstrated that a signiÞcant por- production are common in wing-monomorphic mi- tion of moths captured on Beihuang Island in the gratory species like moths remains unclear (Gate- Bohai Gulf, China during the second early summer house and Zhang 1995, Hanski et al. 2006), though it northward migration were sexually mature and mated has been demonstrated in a few (e.g., Gunn et al. (Zhao et al. 2009). The lack of reproductive habitat on 1989), and is often assumed. A delay in the onset of or near this island demonstrates long-distance ßight of oogenesis, copulation, and oviposition until the end or reproductive females, and reveals unexpected com- near the end of the migratory period, a pattern re- plexity in the relationship between migration and re- ferred to as the oogenesis-ßight syndrome (Johnson production in this species. 1969), is one way migrant insects may manage re- Moth Age and Take-Off. Migration usually occurs source allocation between migration and reproduc- during the preoviposition period of most insects (Ken- tion. The oogenesis-ßight syndrome often has been nedy 1961, Johnson 1969). This appears to be the case considered a basic characteristic of insect migrants for M. separata, at least for initiation of migration (Han (Johnson 1969, Colvin and Gatehouse 1993, Gate- and Gatehouse 1993, Jiang and Luo 2005). Although house 1997, Keil et al. 2001, Gu et al. 2006, Lorenz the preoviposition period of M. separata lasts Ϸ7d, 2007) arising from antagonistic physiological pro- moths are most likely to take off on a migratory ßight cesses. However, it is increasingly recognized that the the Þrst or second night after adult eclosion. This particular tradeoffs in a given species between repro- conclusion is consistent with radar observations 522 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3

Table 1. Comparison of behavioral, morphological, and physiological characteristics of M. separata adults collected in source areas before migration (incipient emigrant populations) and after arrival in receiving areas (immigrant populations)

Character Premigration Postmigration P Flight distance (km) 13.61 Ϯ 17.45 (38) 6.11 Ϯ 9.95 (61) Ͻ0.05 Flight duration (min) 153.05 Ϯ 176.65 (38) 64.26 Ϯ 90.42 (61) Ͻ0.05 Flight velocity (m/s) 5.13 Ϯ 2.15 (38) 4.96 Ϯ 2.96 (61) Ͼ0.05 Dry weight of thoracic dorsal longitudinal muscle (mg/female) 6.53 Ϯ 0.99 (60) 5.84 Ϯ 0.73 (45) Ͻ0.05 Ovariole length (cm) 3.62 Ϯ 0.90 (60) 5.49 Ϯ 1.93 (45) Ͻ0.05 Ovariole width (mm) 0.21 Ϯ 0.11 (60) 0.49 Ϯ 0.15 (45) Ͻ0.05 Ovarium wet weight (mg) 17.05 Ϯ 10.31 (60) 60.46 Ϯ 28.53 (45) Ͻ0.05 Mating frequency (spermatophore per female) 0.22 Ϯ 0.42 (60) 1.02 Ϯ 0.34 (45) Ͻ0.05 JH II titer (ng/mg) 4.63 Ϯ 2.23 (61) 8.69 Ϯ 6.36 (90) Ͻ0.05 Mating rate (%) 5Ð10 96Ð100 Ñ No. males collected in traps baited with sex pheromonea 0Ð0.03 8.0Ð16.3 Ͻ0.05

a Data are presented as mean Ϯ SD. Number in parentheses is sample size. Probabilities based on t-tests. Data from Jiang and Luo (2005), except from Han et al. (1990).

(Chen et al. 1989) and the relationship between ßight generation in moths ßown on day 1 after emergence behavior and reproduction, which changes as the (Fig. 3, Fig. 4A). Flight on day 1 also was associated adults age (Luo et al. 1999). In tethered-ßight exper- with rapid onset of oviposition and greater reproduc- iments, peak oviposition occurred 1 d earlier in moths tive output. Although corpora allata activity of 1-d old that had ßown than in those that had not. However, ßown moths was comparable to that of unßown moths only moths ßown 1 d after eclosion had signiÞcantly at 12 h after termination of tethered ßight, activity enhanced reproductive capacity through a shortened doubled by 36 h and was 10 times greater by 60 h after female preoviposition period and increased lifetime ßight. However, corpora allata activity of moths ßown fecundity, whereas moths ßown on days 2 or 3 showed on other dayÕs ßight was not signiÞcantly different no enhancement of reproductive capacity. When from those of unßown moths (Fig. 3). Similarly, glyc- moths were ßown for the Þrst time on day 5 after eride content of moths ßown on day 1 was signiÞcantly emergence, their lifetime fecundity was only half that of unßown migrant control moths and less than half higher than that of unßown moths by 1 d after ßight, that of the moths ßown on day 1 (Luo et al. 1999). This and was signiÞcantly elevated as moth age increased pattern suggests that only moths that ßy on day 1 after (Fig. 4A). However, this pattern was not seen after eclosion signiÞcantly enhance adult reproductive ca- tethered ßight of 3 d-old moths (Fig. 4B), and there pacity. Along with the negative effects of ßight on days was even a signiÞcant negative response when moths 4Ð5, this suggests a Þtness advantage to moths taking were ßown on day 5 after eclosion (Fig. 4C). (Li et al., off on days 1Ð2. 2005b). Once again, these results are consistent with A study by Li et al. (2005b) disclosed signiÞcantly an adult sensitive stage within 24 h after eclosion, only accelerated juvenile hormone (JH) synthesis by the in this stage ßown moths can switch into residents by corpora allata and enhancement of energy substrate accelerating JH synthesis and enhancing glyceride

Fig. 3. Mean (ϮSD) activity of the corpora allata in vitro of M. separata females at indicated times after 12-h of tethered-ßight on different days after emergence. Asterisk indicates signiÞcant difference (P Ͻ 0.05) between ßown and unßown females at a given time point (Li et al. 2005b). June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 523

Fig. 4. Mean (ϮSD) glyceride content of M. separata females after 12-h of tethered-ßight on one (A), two (B), or three (C) days after emergence. Asterisk indicates signiÞcant difference (P Ͻ 0.05) between ßown and unßown females at a given time point (Li et al. 2005b). content that result in earlier oviposition and increased ever, in M. separata elevated levels of 3-hydroxya- lifetime fecundity. cyl-CoA dehydrogenase relative to lipid metabolism Flight Performance, Flight Energy, and Flight Mus- produce a ratio to glyceraldehyde-phosphate dehy- cle. Moths from emigrant populations of M. separata drogenase of 1.0Ð1.4 during the course of a long before migration showed greater ßight potential than ßight (Fig. 5B), which suggests that carbohydrates those from immigrant populations after migration ter- continue to be used as ßight fuel in addition to lipids mination. Flight mill experiments showed that ßight (Li et al. 2005a). distance and total ßight duration in the immigrant Another manifestation of a tradeoff in ßight per- populations were signiÞcantly less than those in the formance and reproduction is the difference in ßight emigrant populations, although ßight speed did not muscle development and degeneration before and af- differ (Table 1) (Jiang and Luo 2005). These differ- ter migration. In M. separata, the ultrastructure of the ences in ßight performance between pre- and post- indirect ßight muscle (Luo and Li 1996) shows obvi- migrants are largely attributable to parallel differ- ous muscle growth with increasing age before ovipo- ences in ßight energy substrate reserves and ßight sition, followed by degeneration when the female be- muscle development (Jiang and Luo 2005). The gins to oviposit (Luo 1996). In the Þeld, the dry weight main ßight energy substrates in M. separata are lipids of the thoracic dorsal longitudinal muscles of moths and carbohydrates (Zou et al. 1984, Sun 1986, Cao from emigrant populations was signiÞcantly higher et al. 1995b, Li and Luo 1999). In the early stages of than that of immigrant populations, suggesting partial adulthood, moths mainly use carbohydrates, accom- degeneration of ßight muscles after migration termi- panied by increased activities of enzymes related to nation (Table 1) (Jiang and Luo 2005). Interestingly, carbohydrate metabolism, namely glyceraldehyde- there is evidence that resources reclaimed from ßight phosphate dehydrogenase, glycerol-3-phosphate muscle histolysis may be partially diverted to ovarian dehydrogenase, and lactate dehydrogenase (Fig. 5) development (Li et al. 2001). (Li and Luo 1999, 2005a). However, as moths age, Summary: The Physiological Basis of the Oogenesis- the importance of lipids, especially glyceride, as a Flight Syndrome in M. separate. Together, our evi- ßight fuel increases. In many migratory insects, dence indicates that migration of M. separata usually there is switch from carbohydrates to lipids as fuel occurs prereproductively, and is most likely to be during long-distance ßight (Teo et al. 1987, Rankin initiated during the Þrst two days after adult eclosion. and Burchsted 1992, Sappington et al. 1995). How- During migration, physiological functions related to 524 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3

Nevertheless, the capture of reproductively mature migrants in the midst of a migration event indicates that reproductive development and long-distance mi- gratory ßight are not mutually exclusive physiological processes in this species (Zhao et al. 2009). In that study, reproductively mature migrants were captured in a special island environment which cannot support M. separata colonization because of lack of host plants, and thus the authors could not exclude the possibility that early sexually mature immigrants were forced to remigrate. Nevertheless, the results reported by Zhao et al. (2009), as well as Zhang and Li (1985), empha- size the facultative nature of the syndrome itself, as has been suggested for other species (Sappington and Showers 1992). Therefore, it will be important to de- termine the conditions under which reproductively mature or maturing M. separata individuals engage in migratory ßight, and to identify the cues governing the facultative coupling or decoupling of these physiolog- ically demanding processes in individuals.

Hormonal Control Although insect migratory behavior, ßight metab- olism and reproduction are known to be regulated largely by neuroendocrine factors, such as JH, ecdy- sone (MH), adipokinetic hormone (AKH), and octo- pamine (Rankin 1991), the actual control mechanisms remain unresolved in most species and appear to be diverse owing to the tremendous variety of life history strategies across insect taxa. However, when Johnson (1963, 1969) put forward the hypothesis of the oo- genesis-ßight syndrome as being characteristic of most migratory insects, he also concluded from his review of the literature that both reproduction and migration are regulated by JH synthesized in the corpora allata. This conclusion has been considered essentially cor- rect by other entomologists despite several differ- ences in details of the regulatory process depending on the species (Rankin et al. 1986; Rankin 1991; Dingle 1996; Zera 2004, 2007). JH Homologues and JH Titers Variation in Adults. In M. separata, only JH-I and JH-II, not JH-III, were detected by high performance liquid chromatography (HPLC) (Li 2004). JH titers changed with adult age and developmental stage. JH level is low during the Þrst several days after adult eclosion, when moths are Fig. 5. (A) Glyceraldehyde-phosphate dehydrogenase sexually immature and do not mate, whereas it in- (GAPDH), glycerol-3-phosphate dehydrogenase (GDH), creases signiÞcantly in females at onset of oviposition lactate dehydrogenase (LDH), and 3-hydroxyacyl-CoA (Li 2004). Therefore, JH may be a pivotal hormone dehydrogenase (HOAD) activity in the ßight muscle of M. coordinating adult migration and reproduction. separata pupae and adults of different ages (Li et al. 1999). (B) Enzyme activity in 3-d old females immediately after Relationship Between JH and Flight (migration). tethered ßight of indicated durations (Li et al. 2005a). As mentioned in the section on moth age and take-off, ßight by M. separata can signiÞcantly inßuence JH synthesis by the corpora allata, depending on the age ßight performance, ßight muscle development, and at which the moth is ßown. Radiochemical assays ßight energy utilization are enhanced, whereas repro- indicated that JH biosynthesis rate after ßight in fe- ductive functions such as oogenesis, copulation, and males ßown within 24 h of eclosion was signiÞcantly oviposition usually are suppressed. This situation, higher than that of controls, whereas the rates of those however, is reversed after migration. Therefore, this ßown on days 3 or 5 after eclosion were not enhanced pattern seems to Þt the oogenesis-ßight syndrome or were even depressed (Fig. 3) (Li et al. 2005b). An fairly well. implication of these Þndings is that take-off on a mi- June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 525 gratory ßight on days 1 and 2 after adult eclosion could erogeneity (Vieira et al. 2003, Wilson 1995, Gatehouse signiÞcantly enhance female reproduction. JH titer 1997). (JH-II) in incipient emigrants in the Þeld was signif- Populations reared under similar conditions fre- icantly lower than that of immigrants sampled after quently reveal effects of genes that contribute to dif- arrival (Table 1), regardless of the different geo- ferences in migratory tendency. Quantitative genetics graphic populations tested. Jiang and Luo (2005) also studies indicate a strong genetic role in maintaining suggested that lower JH titers favor adult migration wing polymorphism in the exopterygota (Harrison whereas higher titers stimulate oogenesis. 1980, Dixon 1985, Roff 1986, Solbreck 1986, Roff and JH Associated With Migratory Phase Change Fairbairn 1991, Denno 1994, Masaki and Shimizu 1995, Stressed by Starvation. A recent novel Þnding showed Zera and Denno 1997, Langellotto et al. 2000, Roff and that starving an adult, otherwise destined by larval Ge´linas 2003) and polymorphisms in preovipostion rearing conditions to be a migrant, during the Þrst 24 h period and ßight performance in the endopterygota after eclosion activates JH synthesis by the corpora (Dingle 1986; Gatehouse 1986, 1989; Gunn et al. 1989; allata, which, in turn, accelerates female ovarian de- Gunn and Gatehouse 1993; McNeil et al. 1995). How- velopment (Zhang et al. 2008b). This Þnding may ever, insect migration does not evolve in a vacuum, but expose the hormonal mechanism of adult secondary in a coordinated way with physiological, morpholog- regulation of the decision to migrate in M. separata. ical, behavioral, and other life history traits generating Both JH-I and JH-II titers in the starved moths rose what is called a migratory syndrome (Dingle 2001, earlier and higher than those in the control moths, and 2006). Thus, one would expect natural selection to JH-II titer in the treated females peaked 1 d earlier produce a suite of genetically correlated traits that than in the controls. This earlier peaking of JH-II titers co-evolve with migratory behavior (Dingle 1986, 1996; in the treated moths seems to be the main factor Roff 1986, 1990, 1996). contributing to switching migrants into residents Population Differences. Population genetic studies through accelerating ovarian development while con- of M. separata based on isozymes revealed no signif- straining migratory ßight. icant differences in genetic structuring among differ- JH Analog Function. Direct evidence of JH regu- ent geographical populations in China. However, sig- lation of M. separata migration was obtained from niÞcant heterozygosities among different markers experiments involving injections of JH analog. The across populations demonstrated that high genetic ßight performance of adult moths on ßight mills was variation exists within natural populations (Hao et al. signiÞcantly decreased after injection with JH analog, 1992). High DNA polymorphisms were also found although the effects differed with moth age and sex among individuals within geographical populations at (Luo et al. 2001). Injection of the JH analog led to a ampliÞed fragment length polymorphism marker signiÞcant decrease in glyceride content, thus nega- (AFLP) loci, conÞrming high genetic variation among tively affecting energy reserves available for ßight individuals (Jiang et al. 2007). However, little popu- (Luo et al. 2001). However, it is unclear whether this lation differentiation was found among geographic decreased glyceride content also corresponds to a populations in China, which is likely caused by the negative effect on egg production. When JH analog effects of long distance migration of this species and was injected into female migrants during the adult the resulting high level of population mixing and gene sensitive stage, it clearly induced erstwhile migrants to ßow (Jiang et al. 2007). modify their developmental path into one of repro- Genetics of Preoviposition Period. In M. separata, duction and residency, as evidenced by decreased the adult precalling or preoviposition period can be ßight performance and accelerated reproductive de- used as an index of migratory polymorphism (Han and velopment (L. Zhang, unpublished data). Gatehouse 1993, Luo et al. 2001, Jiang et al. 2005, Zhang et al. 2008a). The preoviposition period ranged from 3 to 8 d among female offspring of moths col- Genetic Control lected in the Þeld when reared under the same con- Insect migration is an important life history adap- ditions in the laboratory, suggesting a substantial ge- tion for escaping and exploiting uncertain habitats that netic component controlling this trait (Jiang et al. is shaped by natural selection, and which plays a key 2005). Parent-offspring regression revealed a narrow role in a speciesÕ evolutionary success (Kennedy 1985, sense heritability for preoviposition period of 0.29, Rankin and Burchsted 1992, Southwood 1977, Gate- demonstrating that genetic factors are responsible for house and Zhang 1995). Evolution of migration less of the variation in female preoviposition period through natural selection of course requires genetic than environment (Fig. 6A). Results of bi-directional variation (Dingle 1986, 1996), and indeed, a large selection experiments also suggest that while a genetic amount of genetic variation in migratory behavior has component must be involved, much of the variation in been detected in populations of migratory insects preoviposition period is environmental in nature (Fig. (Chapco and Bidochka 1986, Roff and Fairbairn 2007, 6B). Reciprocal crosses indicated that preoviposition Jiang and Luo 2007). The genetic basis of insect mi- period is strongly inßuenced by a gene or genes lo- gration can now be investigated using molecular ge- cated on the X chromosome (also called the Z chro- netic markers to detect genetic polymorphisms of mi- mosome in , in which males are the ho- gratory potential that occur in certain insects. These mogametic sex) (Fig. 7), which females inherit from polymorphisms, in turn, can be related to habitat het- the male parent. This Þnding is important, because the 526 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3

Genetics of Flight Performance. Heritability of ßight performance in M. separata was estimated by parent-offspring regression and bi-directional selec- tion (Jiang 2004). Heritability estimates for ßight dis- tance and ßight duration were 0.365 and 0.428, respectively, for mean offspring on mid-parents. Her- itability of ßight distance and ßight duration were estimated by regression of single sex offspring on fe- male and male parent to be between 0.28 and 0.45, demonstrating that Þght capacity has a substantial additive genetic component. However, heritability of ßight distance for offspring on female parents was signiÞcantly higher than that for offspring on male parents, suggesting a maternal effect on ßight distance, although no such difference was found for ßight du- ration. The response pattern of ßight performance from bi-directional selection was asymmetric in long- ßyer and short-ßyer lines. Realized heritability was estimated over one generation as 0.593 and 0.528 for ßight distance and ßight duration, respectively, based Fig. 6. Parent-offspring regression to estimate heritabil- on upward selection but 0.338 and 0.397 on downward ity (A) and response to bi-directional selection (B) of pre- oviposition period in female M. separata. Selection to create selection. However, the realized heritability for the two isofemale lines of long and short preoviposition periods next generation was not signiÞcant. The asymmetry of was initiated on offspring of single females (generation 0) response suggests long-ßyers may evolve more quickly exhibiting long or short periods, respectively (Jiang et al. than short ßyers under the same selection pressure 2005). (Jiang 2004). The high heritabilities indicate that mi- gratory ßight performance is genetically quite labile in precalling (i.e., prepheromone release) period of fe- natural populations. male M. separata is also X-linked (Han and Gatehouse Genetic Correlation Between Flight and Reproduc- 1991b). It is possible that these two traits are deter- tion. On the basis of estimated heritability in preovi- mined by the same gene, that two different genes for position period and ßight performance of M. separata, these traits are both located on the X chromosome, or genetic correlations between ßight performance and that autosomal genes for the traits are regulated from reproduction were studied by means of artiÞcial se- the X-chromosome as part of the suite of characters lection (Jiang 2004). Bi-directional selection strongly comprising a migration syndrome in this species. evidenced the existence of additive genetic covari-

Fig. 7. Distributions of preoviposition period of female offspring of intraline and reciprocal crosses between isofemale lines of M. separata selected for early (EO) and late oviposition (LO) (Jiang et al. 2005). June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 527 ance between ßight performance (ßight distance and migrants that were starved in the adult sensitive stage. duration) and reproduction (preoviposition period The relationship between AT mRNA expression level and total fecundity). and JH titers was strongly correlated, although mea- Genetic correlation coefÞcients between preovipo- sures differed slightly depending on the technique. sition period and ßight distance or ßight duration were Haemolymph JH titers of starved females for the most 0.326 and 0.228, respectively, indicating that ßight per- part were greater than in the controls. Relative AT formance is positively correlated with preoviposition expression was higher in starved moths through 4 d period. In contrast ßight performance was negatively after treatment, and appeared to be positively corre- correlated with lifetime female fecundity, with ge- lated with JH titer during that period (Zhang et al. netic correlation coefÞcients of Ϫ0.323 and Ϫ0.225 for 2008b). Based on these results, we proposed a model distance and duration respectively. Increased ßight of the hormonal and physiological mechanisms un- performance accompanied by delayed oviposition and derlying the shift of migrants into residents during the less fecundity (Jiang 2004), are expected to result in adult sensitive stage. Starvation during the adult sen- a lower population growth rate. In contrast, local res- sitive period (i.e., Þrst day after eclosion from the idents show early reproduction and high fecundity ) leads to increased AT levels, which then stim- (Jiang 2004), suggesting a genetic trade-off between ulates the corpora allata to synthesize JH. An increase ßight performance and reproduction, partly mani- in hemolymph JH accelerates ovarian development fested as the oogenesis-ßight syndrome. and ßight muscle degeneration, although the thresh- old titer of JH to trigger these results remains un- known. This model is consistent with the results of Molecular Control previous related environmental, physiological, and Molecular studies provide a deeper understanding hormonal studies (Luo et al. 1995a,b, 2001; Jiang and of the mechanisms regulating insect migration. These Luo 2005; Zhang et al. 2006), and is supported by include, for example, studies on functional proteins studies of other insects (Rankin and Ridifford 1978; such as ßight muscle-speciÞc actin and myosin which McNeil et al. 1995, 2000; Zera 2004). control insect ßight apparatus development (Liu et al. AT Function in Switching Migrants Into Residents. 2003), enzymes and binding proteins controlling ßight To further illuminate the biological function of the AT energy metabolism and hormone synthesis (Gunn and neuropeptide in switching migrants into residents, pu- Gatehouse 1988, de Kort and Granger 1996), and neu- riÞed recombinant AT was microinjected into migrant ropeptide and receptor proteins controlling hormone M. separata during the adult sensitive stage (Zhang synthesis and release (McNeil and Tobe 2001, Zera 2006). A bacterial expression vector of pET/AT was 2004). In an expressed sequence tag study, Kang et al. constructed, and SDS-PAGE results showed that it (2004) identiÞed several hundred differentially ex- was successfully expressed in Escherichia coli. After pressed genes associated with gregarious (migrant) optimizing the conditions for inducing expression, the and solitary (resident) phase migratory locusts. The recombinant protein with a HIS-tag was puriÞed and neuropeptides allatotropin (AT) and allatostatin, collected. Injection of female migrants in the sensitive which regulate JH titers, and JH esterase, which hy- stage with puriÞed recombinant AT protein signiÞ- drolyzes the methyl ester of JH and alters its activity, cantly decreased preoviposition period and acceler- have attracted the attention of entomologists inter- ated reproductive development, while decreasing ested in regulation of insect migration because of the ßight performance. Control female migrants treated signiÞcant role JH plays in both ßight and reproduc- by pET21-b bacterial expression product alone and/or tion (McNeil and Tobe 2001). acetone were not signiÞcantly affected compared with AT Gene Clone and Characterization. A full-length the untreated controls. These results demonstrate that cDNA encoding AT from M. separata (Mytse-AT) was the effects of starvation on switching migrants to res- cloned and characterized by RT-polymerase chain idents is modulated by a release of the AT neuropep- reaction (PCR) and the RACE technique (GenBank tide. Although JH titers were not measured after AT accession no. DQ208707) (L. Zhang, L. Luo, and X. microinjection, the results are consistent with the pro- Jiang, unpublished data). Mytse-AT is encoded by a posed model of regulation described above (Zhang 136 amino acid precursor, with a calculated molecular 2006). weight of 15.385 kDa. The sequence of amino acid residues 39Ð52 of the mature Mytse-AT peptide was Summary and Future Challenges completely identical to that of the puriÞed Manduca sexta AT peptide (Kataoka et al. 1989) and its cDNA Overall, the process of migration in M. separata sequence (Taylor et al. 1996). The Mytse-AT precur- across take-off, transfer and termination is wondrously sor is 97% similar to that of the 135 amino acid pre- complicated, and is regulated by a number of ecolog- cursor of Pseudaletia unipuncta AT (Truesdell et al. ical, physiological, hormonal, genetic, and molecular 2000). factors (Fig. 8). This species balances several potential Relationship Between AT and JH Stressed by Star- selective advantages and disadvantages of migration vation. Zhang et al. (2008b) used HPLC, semiquanti- by coordinating an array of behavioral, physiological tative RT-PCR and real time quantitative PCR tech- and genetic strategies. For example, although annual niques to examine the relationship between JH titer multi-generation round trip migrations between and expression of the AT gene in female M. separata southern and northern China are predictable and 528 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 3

Fig. 8. Flowchart of the primary regulation of migration of M. separata, which occurs in the larval stage, and secondary regulation of migration, which occurs during the Þrst day of the adult stage. characteristic of M. separata, a small portion of pop- logenin deposition. However, these factors are acti- ulations leave behind residents that breed locally. vated to both suppress adult ßight and stimulate re- Among those that migrate, the oogenesis-ßight syn- production when adult migrants in the sensitive stage drome harmonizes the competing physiological de- encounter any of several environmental conditions mands of adult ßight and reproduction. Genetically, such as starvation, low temperature, and long photo- offspring inherit parental additive genetic effects gov- period. Based on a number of experiments, we hy- erning migratory behavior. However, they also retain pothesize that the mechanism behind this switch is ßexibility in expression of both ßight and reproductive activation of neurosecretory cells to release the neu- life history traits, as evidenced by abundant genetic ropeptide AT, which stimulates the corpora allata to variability between individuals in the Þeld and a high biosynthesis JH. Release of JH then results in ßight environmental inßuence. Therefore, populations per- muscle degeneration and vitellogenesis. sist and grow despite harsh and changing environ- It is not surprising that environmental factors ex- ments. perienced by larvae can determine the developmental One of our most unexpected discoveries is that pathway into either adult migrants or residents, but there is a developmental window allowing secondary our discovery that migrants have a second decision regulation of migration potential in this species during point allowing a switch into residents suggests a much the adult stage (Fig. 8). The initial facultative decision more complicated strategy for attaining optimal Þtness to develop into a migrant or resident is made during in a given generation. Thus, we propose that adults of the larval stage. However, there is a short sensitive M. separata develop as migrants or residents according stage occurring within 24 h after adult eclosion when to environmental cues received before eclosion, and a nonreproductive migrants can be induced to switch to decision to be a resident is irreversible. However, if reproductive residents. During the sensitive stage, certain conditions have changed sufÞciently within adult corpora allata and the AT neuropeptide are not 24 h after eclosion, migrants readjust their behavioral activated and there is no JH biosynthesis and vitel- strategy to remain and reproduce locally. The evolu- June 2011 JIANG ET AL.: REGULATION OF MIGRATION IN Mythimna separata 529 tionary consequences of this unusual phenomenon are Cai, B., X. F. Jiang, L. Z. Luo, Y. Z. Cao, and Y. Q. Liu. 2002. not yet clear. We speculate that although extreme Inßuences of temperature and humidity on utilization of environmental cues experienced by the young adult, energy substance during ßight in the moths of oriental such as lack of nectar or cold shock, would seem armyworm, Mythimna separata (Walker). Acta Ecol. Sin. predictive of poor reproductive conditions, they also 22: 114Ð121. seem predictive of poor migration conditions, and the Canavoso, L. E., Z. E. Jouni, K. J. Karnas, J. E. Pennington, and M. A. Wells. 2001. Fat metabolism in insects. Annu. decision to stay and reproduce may be the less risky Rev. Nutr. 21: 23Ð46. strategy. This idea would be consistent with a migra- Candy, D. J., A. Becker, and G. Wegener. 1997. Coordina- tory strategy that evolved primarily to exploit and tion and integration of metabolism in insect ßight. Comp. colonize new habitat, rather than to escape deterio- Biochem. Physiol. 117B: 475Ð482. rating habitat. Cao, Y. Z., K. Huang, and G. B. Li. 1995a. Inßuences of Although our understanding of the cellular and mo- ambient ßight humidity on ßight movement of the ori- lecular mechanisms underlying the regulation of mi- ental armyworm Mythimna separata (Walker). Acta Phy- gration in M. separata are clearly in their early stages, tophyl. Sin. 22: 134Ð138. this is, in part, a reßection of the complexity of this Cao, Y. Z., L. Z. Luo, G. B. Li, and Y. Hu. 1995b. The speciesÕ migratory process. We hope that this frame- relationship between utilization of energy materials and sustained ßight in the moths of oriental armyworm, My- work will have some value in further elucidating reg- thimna separata (Walker). Acta Entomol. Sin. 38: 290Ð ulatory mechanisms. Similar research on molecular 295. protein structure and function on allatostatin, protho- Cao, Y. Z., L. Z. Luo, and J. Guo. 1996. Performance of adult racicotropic, and prothoracicostatic hormones, ßight reproduction and ßight in relation to larval nutrition in muscle actin, key enzymes involved in the JH and the oriental armyworm, Mythimna separata (Walker). ecdysone synthesis pathway and in ßight energy me- Acta Entomol. Sin. 39: 105Ð108. tabolism, lipid binding proteins, as well as hormone Cao, Y. Z., G. B. Li, and Y. Hu. 1997. Effect of photoperiod receptors should be strengthened. Novel molecular on reproduction and ßight of oriental armyworm, My- techniques such as RNA interference, gene knock thimna separata (Walker). Acta Entomol. Sin. 17: 402Ð down and genetic engineering should also be ex- 406. Chapco, W., and M. J. Bidochka. 1986. Genetic variation in plored. Insect migration research has been focused prairie populations of Melanoplus sanguinipes, the migra- mainly on environmental inßuences and mechanisms tory grasshopper. Heredity 56: 397Ð408. on regulation of the migratory process during ascent Chen, R. L., and X. Z. Bao. 1987. Research on the migration and descent. However, few biological factors such as of oriental armyworm in China and a discussion of man- natural enemy intimidation effects and regulatory agement strategy. Insect Sci. Applic. 8: 571Ð572. mechanisms during the transport phase of migration Chen, R. L., X. Z. Bao, V. A. Drake, R. A. Farrow, S. Y. Wang, have been investigated. Only after we have explored Y. J. Sun, and B. P. Zhai. 1989. Radar observations of the the environmental and biological factors involved in spring migration into northeastern China of the oriental stimulating and controlling the entire migratory pro- armyworm, Mythimna separata and other insects. Ecol. cess, including take-off, transport and termination, can Entomol. 14: 149Ð162. Chen, R. L., Y. J. Sun, S. Y. Wang, B. P. Zhai, and X. Z. Bao. we achieve a holistic understanding of the ecology and 1995. Migration of the oriental armyworm Mythimna evolutionary underpinnings of migration as a life his- separata in East in relation to weather and climate. tory strategy in this species. I. Northeastern China, pp. 93Ð104. In V. A. Drake and A. G. Gatehouse (eds.), Insect Migration: Tracking Re- source in Space and Time. Cambridge University Press, Acknowledgments Cambridge, United Kingdom. Chen, S. D., and B. H. Hu. 2000. Plant protection in China We thank the USDA-ARS Corn Insects & Crop Genetics in Þfty years. Agriculture Press, Beijing, China. Research Unit for providing XFJ an opportunity to present Cheng, X. N., J. C. Wu, and F. Ma. 2003. Brown planthopper his laboratoryÕs cumulative research on this topic at the 2009 occurrence and control. China Agricultural Press, Bei- NCERA-148 meeting in Virginia, which generated valuable jing, China. feedback and encouraged this reviewÕs composition. This Chin, T. S., H. Chung, and S. C. Ma. 1964a. 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