Open access peer-reviewed chapter
Abstract
This chapter is a review of data on structure, diversity and adaptive properties of seasonal cycles in ants. Most tropical ants demonstrate homodynamic development. They do not show any developmental delays and all-year round the ontogenetic stages from egg to pupa exist in their nests. Some of the quasi-heterodynamic species have permeated into the regions with warm temperate climate but a true diapause did not evolve. Most temperate and all boreal climate ants are true heterodynamic. They manifest a real winter diapause (prospective dormancy) in their annual cycle. Thus, a variety of forms of dormancy, which were found in ants, extend from elementary quiescence to deep diapause. Heterodynamic ants use two main seasonal strategies with respect to brood rearing: strategy of concentrated brood rearing (Formica type) and strategy of prolonged brood rearing (Aphaenogaster type, Myrmica type). The larval stages at which diapause can occur are extremely variable among ants. The evolution of seasonal life cycles and possible ways of origin of diapause in ants are discussed. The subtropical (quasi-heterodynamic) and tropical (preadaptational) evolutionary paths to true heterodynamic development are considered. It is concluded that similar seasonal adaptations could arise in the evolution of ants independently many times and usually are not tightly bound to the taxonomic position of species.
Keywords
- Formicidae
- ants
- seasonal development
- life cycles
- homodynamic
- heterodynamic
- diapause
- exogenous
- endogenous
- temperature
- climate
- evolution
1. Introduction
The life of ants as ectothermic organisms is closely connected with the seasonal variations of ecological factors, such as temperature, rainfall, humidity, availability of food, etc., occurring during the year. Certain climatic changes usually manifest even in tropics and cause the corresponding modifications in behavior and development of ants and other insects, but they are much more pronounced on the north. In the regions with temperate and boreal climate, the annual changes of climatic conditions possess a hard impact to the life cycles of all organisms living there. In different ant species, various annual cycles of behavior arise. They have been described in many reviews (for example, see [1, 2]). However, the seasonality of the behavioral cycle in ant colonies is strictly subordinated to the seasonality in developmental processes such as oviposition or larval rearing. Each ant species demonstrates certain annual developmental cycle because the processes of the colony development cannot proceed without interruption during the whole year.
To optimize the survival and growth of ant colonies, the entire warm season should be used for larvae rearing and for production of the greatest quantity of new adults. That is why the brood development should start in spring as earlier as feasible and prolong as longer as possible in late summer. At the same time, only the brood stages that are able to survive during the winter should occur in ant colony by the end of autumn. To ensure this, the special physiological mechanisms evolved which provide synchronization of the colony development with the yearly climatic periodicity.
The first investigations devoted to seasonality in the development of ants were performed by Yozhikov who studied the phenology of the development in several ant species from Central Russia [3]; by Headly who characterized the seasonal development of two
Despite extensive studies of arthropod dormancy and seasonality, myrmecologists paid very little attention to the role of seasonality in ant ecology, as well as in the evolution of the life cycles of these social insects. Literature on this topic is not rich. Quite a few publications specifically devoted to seasonal development and the phenology of ants. As a rule, such data can be found in the investigations dealing with the biology and ecology of certain species. Even less frequently, the subject of the study was the regulation of annual cycles of the ant development. Most often, these problems were affected accidentally and stood in the background and pushed back by the main aims of the study (for example, see [8]). The seasonal development of the ants
This paper contains a review of literary and proprietary data on the structure, diversity, adaptive features and evolution of seasonal cycles and strategies of the seasonal development in ants. We have studied the seasonal cycles in more than 80 species belonging to more than 20 genera from different regions of Russia and the former USSR, ranging from warm temperate to cold temperate and boreal climatic zones. Our field and laboratory studies have allowed us to map the diversity of annual cycles, to reveal the underlying ecophysiological and social mechanisms of control and to develop ideas on possible pathways in the evolution of the seasonal cycle in ants.
The main study methods we have used were laboratory experiments and field phenological observations. In experimental studies, the ant colonies were divided into fragments each consisted of workers, queens and the brood. In the case of a small number of workers in the colony or for monogynous species with a single queen in the nest, entire natural colonies were used. Colony fragments (or the whole colonies) were kept in artificial plastic nests, which were randomly distributed over various experimental regimes (different photoperiodic conditions and constant temperatures or thermal periods) and experimental regimes were maintained in special thermostats. Our methods of laboratory cultivation of ants provided the opportunity to observe and to study all stages of annual cycle including the overwintering in a refrigerator under the temperatures of 3–5°C.
2. Peculiarities of seasonal development in ants as social insects
In social insects, in addition to the life cycles of individual individuals, there is a life cycle of the colony, as an integrated, superorganismic system. It consists of the processes of the development of individuals, but it is not equivalent to a simple summation of them. Social regulation mechanisms arise in the evolution and are realized through interactions between members of the colony. They control the physiological state and the development of individuals, depending on the ecological situation and colony needs. Such “collective regulation” of development is absent in solitary species and largely determines the specificity of seasonal development in ants [11, 12, 13, 14, 15, 16].
Colonies of ants are not only perennial but usually have unlimited life cycle under favorable conditions of environment [17]. Not only queens but even workers can survive for several years. In monogynous species, all workers and the brood are the offspring of the only queen. So while the queen is alive, all the population of a colony can relate to one and the same genetic generation during consistent years. In polygynous species with several queens in a nest, all individuals inhabiting a single colony may pertain to various generations which overlay each other. However, the seasonal life cycle of the colony is not associated with differences arise between generations. It embraces the regular seasonal variations in physiological state of all individuals in a colony which entail the orderly changes in behavioral and developmental patterns. Therefore, we determined the seasonal life cycle of an ant colony as the annual cycle of physiology, behavior and development [18].
After the spring awakening, the queen commences laying eggs, the development of larvae begins and pupae appear. There are workers and reproductive individuals among new adults. Oviposition and brood development continue throughout the warm period of the year and cease in the autumn, when insects begin to prepare for wintering, go to special shelters and spend the winter in inactive state. The annual cycle of colony development is a collective and highly organized process and includes the individual development of immature stages (the brood) and regular seasonal changes in the physiological state and reproductive activity of adults (workers and queens).That is why the growth and development and the beginning and termination of diapause in ants can be considered and studied both in individual level and at the level of the entire colony. And this is not the same thing, since all these processes are under the control of the mechanisms of social regulation and integrated reactions of the colony to the changes in environmental conditions. In this connection, diapause of ant larvae can be (and usually happens) facultative at the level of an individual, but at the same time obligatory at a colony level (in endogenous-heterodynamic species).
3. Homodynamic type of seasonal development
On the general background of an insufficient study of the phenology in ants, the tropical regions of the Earth are especially prominent. Analysis of meager data shows that at any time of the year, in the nests of most tropical species studied, all the stages of ontogenesis from the egg to the pupa are present, and development retardations are absent. Such continuous all-year round development without the obligatory onset of periods of physiological dormancy we call homodynamic, using the terminology of E. Roubaud [18, 19, 20, 21].
However, homodynamic species often have a certain seasonal structure of the annual cycle: on a general background of continuous development, there may be significant seasonal fluctuations in the number of certain ontogenetic stages, as well as seasonal association of the rearing of alates and nuptial flights. Thus, in
In addition, periodicity of oviposition was noted for a number of species. For example, in the natural colonies of
The homodynamic development of some tropical ants was observed in the laboratory. G. Terron maintained colonies of the African species
We observed homodynamic development in two species from tropics:
It is well known that typically tropical insects cannot survive for a long time at temperatures well below the optimum and, especially, below the developmental threshold [44]. Therefore, it can be argued that the tropical ants in their majority are not adapted to survive during the cold periods of the year. However, some ant species can demonstrate continuous all-year round development even in subtropical environments. For example, in the central regions of Texas (USA),
4. Heterodynamic cycles of development
Annual developmental cycles of ant colonies, in which a diapause arises naturally, we call after Roubaud heterodynamic [18, 19, 20, 21]. They have a distinct seasonal structure: the period of diapause (the phase of dormancy) is regularly replaced by the period of development (the active phase of the cycle), after which a new period of diapause occurs, and so on. Generally, the phase of dormancy in the annual cycle coincides with the period of unfavorable climatic and (or) food conditions. It is characterized by a lack of larval development and, as a rule, of queen oviposition and the presence in the nests of only certain (usually diapausing) brood categories. During the active phase of the annual cycle, eggs are laid and the larvae are reared. Ants grow up new workers, as well as alate females and males.
4.1. Quasi-heterodynamic development
Some ant species recently penetrated from tropics or subtropics to areas with a warm temperate climate and successfully settled there. Two species of fire ants,
Several authors have shown that in southern United States (Mississippi, Florida, South Carolina, etc.) both fire ant species remain essentially homodynamic: eggs, larvae and pupae of workers are present in their nests all-year round [48, 51, 52]. However, the number of immature stages varies considerably during the year, and in winter, it is very small. In February–March, the number of eggs increases sharply and new larvae develop and begin to pupate in April (workers) and May (alates). At this time, the quantity of brood categories is maximal and reaches 40–45% of the entire biomass of the colony. Reproductive individuals appear from pupae in June and fly out of the nests at least five times during the summer. The second small peak of the brood population (up to 35% of the biomass) in the nests coincides with the first cooling in September–October. At this time, all larvae and pupae belong only to the caste of workers. In November–December, the number of larvae and pupae sharply decreases and reaches a minimum (less than 2% of the biomass of the colony) in January. Thus, the number of immature stages in fire ants directly depends on the environmental temperature.
It has been determined that in the most northern populations of
Such tropical species, adapted to live in regions with cold winters without forming real diapause, we call quasi-heterodynamic [18]. They are characterized by the potential for unlimitedly long development under favorable conditions inherent in homodynamic species. The development of their brood ceases only at temperature below the developmental threshold and ants spend the winter in a quiescent (cold coma) state suffering from more or less strong mortality, but in general the colonies overwinter successfully.
The Argentine ant
Since the fire ants and Argentine ants recently permeated to the areas with cold winters, we tend to think that they do not yet have diapause. However, it has been experimentally determined that only the overwintered colonies of the Argentine ant can grow up a lot of alate females, which appear in the nests in the south of France at the beginning of the summer season [57]. This suggests that there are seasonal changes in the physiological state of colonies that are similar to diapause.
According to the literature date, many subtropical ants do not have any brood in their nests during the winter, for example,
We discovered and investigated quasi-heterodynamic developmental cycles in several ant species living in regions with subtropical and warm temperate climates. In the colonies of
In the experiments on
Two
For
When we decreased the keeping temperature for the autumn colonies of
4.2. True heterodynamic development
Most temperate and all boreal climate ants are true heterodynamic. They possess real winter diapause in their annual cycles (prospective dormancy) [18]. The presence of this diapause provides a more successful wintering by increasing the physiological resistance of larvae and adult ants to unfavorable winter conditions. In the literature, there is practically no data on the tolerance of developing and diapausing larvae, other developmental stages and adult ants to low temperature and other unfavorable environmental factors. Plateaux [69] noted that
True heterodynamic seasonal cycles occur in the vast majority of ant species living not only in temperate and cold climates, but also in subtropics and even in tropics. The presence of long-term developmental delays was noted, for example, in all five species from the
It is clear that for the occurrence of heterodynamic development in tropics, any seasonal changes in environmental conditions have to exist. Since the annual rhythm of the climate is usually quite distinct in the tropical regions, and its absence, on the contrary, is very rare situation, heterodynamic seasonal cycles should probably be widespread in tropical ants. The hibernation and diapause are widespread in tropical insects, but mechanisms of the regulation of heterodynamic cycles in tropics are far from understanding and explaining yet [70].
It should be assumed that heterodynamic development is more common for ants in subtropics, because the seasonal rhythm of the climate there is much more pronounced than in the tropical zone. Indeed, most of the subtropical species studied demonstrate the cessation of development in winter. Some of them do not have brood, while others overwinter with larvae:
5. Two seasonal strategies of brood rearing in heterodynamic ants
Analyzing the structural diversity of heterodynamic seasonal cycles in ants, we identified two fundamentally different directions in their evolution, and accordingly, two seasonal strategies for brood rearing [18].
5.1. The strategy of prolonged brood rearing
The ants are more likely to follow the strategy of prolonged brood rearing. This strategy is based on the ability of larvae to enter into a diapause and to continue development over the next summer (Figure 1). Depending on the composition of the overwintering brood and the stage at which diapause is observed; we distinguish two structural types of developmental cycles [80].
Figure 1.
The strategy of prolonged brood rearing. Further explanation in the text.
The annual cycles of ants that overwinter with brood have the most complex seasonal structure (Figure 1). All hibernating larvae usually pupate during the summer season. They give the first peak in the number of pupae in the nests. As a rule, alate females and males develop from most of them. Some of the larvae that emerged from the eggs which were laid in spring and early summer can pupate during the same growing season. This is the so-called a rapid or summer brood, according to Brian [81, 82]. It develops without diapause and gives the second peak in the number of pupae. All other larvae that emerge from the eggs within the season, fall into a diapause, hibernate and finish their development only next summer. This is so-called a slow or winter brood [81, 82]. Thus, two complete cycles of brood development from the egg to imago take place in a colony during each year (Figure 1): a summer cycle that begins and ends within one growing season, and a winter cycle, in which larval development is interrupted by their diapause.
Rapid brood is found in most species from the temperate zone. It may be absent in species and populations from the northern regions, where summer is short, as well as in species with very slow individual development. For example, the rapid brood is absent in
The strategy of prolonged brood rearing is extensive inherently, as it is realized by stretching of the development of individuals for two or more summer seasons. The appearance of larval ability to fall into a diapause gave the ants a unique way for adaptation to the life in a temperate climate and especially in high latitudes. Therefore, the strategy of prolonged development is most common among the ants living there. It has a number of adaptive advantages.
5.1.1. More complete use of a favorable period for the development and available thermal resources
Since the larvae are always in the nest, the workers can feed them from early spring to late autumn. Immediately after the end of the winter, as soon as it becomes a little warmer, the ants carry larvae from the underground chambers to the upper, warmed by the sun, horizons of the nest (beginning with the largest larvae), creating the best opportunity for larval growth and development. As it becomes warmer and the amount of available food increases, the ants carry more and more small larvae to the upper levels of the nest and begin to feed them. According to Peakin for
The autumn period of larval rearing is also of great importance for most ants with a wintering brood. For example, in the central part of European Russia in the colonies of
Thus, in the species using the strategy of prolonged brood rearing, workers are engaged in feeding of larvae until the final onset of cold weather and give them all the surplus food produced during this period (minus the amount of nutrients that the workers accumulate in their fat body). This makes it possible to maximize the total mass of the wintering brood and, consequently, to grow up earlier the first workers, as well as reproductives, next spring. In addition, the biomass accumulated by larvae is also a reserve of nutrients for the colony: in the case of food shortage, ants can eat a part of the brood (mainly eggs and small larvae) in order to survive and to feed the largest larvae [2, 87].
5.1.2. The ability to adapt to the duration of the warm period of a year by changing the amount of the rapid brood
Such adaptation path can be realized during the penetration of the ants into more northern areas [88] and in connection with the local variability of climatic conditions from year to year. In the north, where summer is short and heat resources are limited, the ants can grow up much less number of the rapid brood than in the south. For example, in the south of France,
In the far north, where the summer is even shorter and the warmth is even less than in St. Petersburg, the ants generally never have rapid brood [88]. This was demonstrated in our studies on
5.1.3. The ability to stretch the development of larvae for two or even three summer seasons
Lack of thermal and/or nutritional resources during the summer is not uncommon situation in areas with cold temperate climate. As a result, some overwintered larvae that do not reach the size sufficient for pupation, fall into a diapause repeatedly and hibernate the second time. Repeated overwintering of some larvae was noted for
However, the number of larvae repeatedly overwintering probably cannot be significant in the colony. This is hampered by some social factors that limit possible changes in the structure of the seasonal developmental cycle when ants penetrate into more northern regions [88]. Therefore, ants never go over to the opportunistic strategy of stretching development for several years, so typical for many boreal and arctic insects [94, 95]. This feature restricts further spread of ants to high latitudes.
5.2. The strategy of concentrated brood rearing (Formica type)
This strategy presumes the obligatory completion of the development of larvae emerging from the eggs during one summer season, i.e. is typical for species that hibernate without brood (Figure 2). We named such annual cycles as
Figure 2.
The strategy of concentrated brood rearing. Further explanation in the text.
After the onset of queen diapause, new eggs stop to appear and all existing brood gradually completes development. The diapause of queens should not occur too early, otherwise the period available for brood development would be actually reduced. Simultaneously, if diapause arises too late in the season, many larvae and pupae would be caught by the onset of winter and destroyed by the cold. That is why the moment when queens enter into a diapause is the most important for the
Our studies have shown [42, 96] that this is really so: in
According to our data, at temperatures of 25–26°C close to optimum temperatures for
Thus, it can be assumed that raised rate of ontogenesis in
6. Review of heterodynamic annual cycles in ants
6.1. Seasonal cycles of Aphaenogaster type
For the first time, the seasonal cycle of ants of the genus
We found and investigated this annual developmental cycle on
Thus, of all the currently known ants from the temperate climate going on hibernation with eggs, they probably overwinter happily only in the
Despite this, in subtropics and in areas with a very warm temperate climate, where winters are mild and short, seasonal cycles of
Most species of the genus
6.2. Seasonal cycles of Myrmica type
The first studies of annual cycles of such type were fulfilled in the USA by Headley on two
The first study, in which the annual cycle of development was observed in the laboratory, belongs to Brian [81]. He maintained two colonies of
The larval stages, on which the diapause can occur, are extremely variable among ants with
6.2.1. Diapause in early (1st–3rd of 5 or 6) instars (Lepisiota, Plagiolepis, Tapinoma and some Camponotus )
Larvae of the first three instars hibernate in
Diapause in early instars is also typical for many
6.2.2. Diapause in middle (2nd–4th of 5–6) instars (Camponotus s. str .)
Sanders indicated that in
6.2.3. Diapause in the late (3rd–4th of 4) instars (Harpagoxenus, Leptothorax, Temnothorax and Messor )
According to the literature data, the larvae of
Our investigations demonstrated that in
6.2.4. Diapause in the last (usually 3rd) instar (Manica, Diplorhoptrum, Leptanilla, Monomorium, Myrmica, Tetramorium )
Only larvae of the third (last) instar hibernate in all
Larvae of the ants, hibernating at the last instar, are for the most part far from the completion of development, i.e. they are at the beginning or in the middle of this stage. To achieve the size required for pupation, they usually need a fairly long period of growth after overwintering. This fully applies to the largest of overwintering larvae that develop in spring into alate reproductives. An exception to this rule
6.2.5. Diapause in all (of 3–6) instars (sometimes except the first instar) (Aphaenogaster, Crematogaster, Lasius, Paratrechina, Camponotus , Tanaemyrmex )
This group includes
6.3. Seasonal cycles of the Formica type
According to the literature data and own observations, this annual cycle is typical for the ants of the entire tribe Formicini (genera
Outside the tribe Formicini, annual cycles without wintering brood were found in
We found the annual cycle of
7. Two types of the regulation of heterodynamic annual cycles
The main characteristic feature of homodynamic and quasi-heterodynamic types of annual cycles is a purely exogenous control of the development, and the key factor is environmental temperature. Heterodynamic species have a much more complex regulation of seasonal development, usually based on a combination of exogenous and endogenous mechanisms. We divided all heterodynamic ants into two groups, which differ substantially in the principles of the regulation of the annual cycle, exogenous-heterodynamic species and endogenous-heterodynamic species [18].
The first of them is characterized by the possibility of continuous and unlimited development under optimal conditions. The diapause is optional and occurs only when the temperature is lowered. Such annual cycles we call exogenous-heterodynamic. They are typical for all species of the genera
Thus, exogenous-heterodynamic species are distinguished by facultative winter diapause in larvae and queens. Developmental delays in a colony are purely exogenous and ensue as a straight reaction to the influence of external environmental factors, primarily, of temperature when it becomes not optimal for the development. Moreover, inhibition of development is unstable and easily disrupted when the temperature rises. However, these developmental delays are not just a consequence of cold coma but, namely, are the form of diapause (for more details, see [18]). This is not a state of elementary quiescence as in species with quasi-heterodynamic annual cycles, because this kind of diapause starts when environmental temperature still significantly exceeds the developmental threshold. Other essential feature is that the diapause arises not directly after the temperature decline but with some lag. Additionally, this diapause is invertible and may be terminated or induced again several times by consistent rising or decreasing the temperature, but each time after a little delay. The second important property of exogenous-heterodynamic species is the distinct change of their reaction to temperature during overwintering as a result of cold reactivation. After natural overwintering or after exposure in a refrigerator to 3–5°C during 2–3 months, the development and pupation of larvae recommenced and proceeded for a long period at 20°C and even at 18°C (in some
Most of the ants from temperate zone belong to the second group of species which is characterized by endogenous-heterodynamic annual cycles. The diapause arises due to internal factors (endogenous timer) and no external conditions can prevent it [18, 145]. Even under long day conditions and optimal temperatures, including the diurnal thermal periods, which are the most favorable thermal conditions for ants [146, 147, 148], the development in colonies of these species necessarily ceases, and the phase of dormancy in the annual cycle begins.
Thus, the diapause of endogenous-heterodynamic species is obligatory for the colony which has an internally limited intrinsic seasonal cycle of brood rearing. External environmental factors, such as temperature and photoperiod, also participate in the regulation of annual cycles of these species, playing a corrective role, i.e. in varying degrees adjusting the duration of the cycle to the climatic peculiarities of a particular summer season. But the regulation of the cycle is still based on processes that are endogenous for the colony [18, 145]. According to our data, the following species living in temperate climate belong to the group with endogenous-heterodynamic annual cycles:
The gradual decrease of a colony capability to produce new eggs and to grow up non-diapausing larvae takes place during the summer season. At the same time, there is the increase of the bias for diapause as a consequence of the ongoing endogenous physiological and social processes. Moreover, the ant colony gradually acquires the sensitivity to the day length (to the photoperiod). The increasing photoperiodic sensitivity of a colony strongly changes the reaction to temperature. Because of these processes, at the end of the summer, the decrease of temperatures and the shortening of the day length (in some species only) contribute to the onset of diapause, thereby reducing the period of egg laying and larval development. The same impact of external factors to the colony’s life cycle was found in all ant species that we studied [80, 96, 146, 163, 164, 165]. So, the duration of a colony’s annual cycle of brood rearing in nature is controlled both by an endogenous timer and by exogenous environmental cues, such as temperature and photoperiod (in some species). These environmental conditions adjust the date of diapause onset to the climatic features of a given year.
Temperature control of diapause is the most universal in ants. The higher temperatures delay the onset of diapause both in larvae and adults, whereas the lower temperatures always accelerate the process of the beginning both in larvae and adults. On the contrary, photoperiodic control of diapause is unexpectedly uncommon among ants. For the first time, the photoperiodic responses were revealed in
The subsequent extensive investigations nonetheless have shown that apart from
Thereby, the seasonal development of most ant species from temperate climate regions depends on inner timer in combination with environmental temperature, which triggers the onset of diapause. The environmental factors can modify the duration of the seasonal brood-rearing cycle within broad range in most species of the genera
The seasonal cycle of oviposition and development in other species is controlled predominantly by the endogenous mechanisms. In these ants, the moment of diapause onset depends only slightly on environmental conditions. Temperature hardly modifies the intrinsic length of the queens’ oviposition period in all studied
8. The regulation of diapause in larvae
The diapause of larvae in ants is facultative in most case, i.e. a given larva can either develop directly or fall into a diapause depending on the circumstances. Temperature can affect larval development and induce diapause both directly and through the nurse workers. Detailed studies performed on
The results of these experiments demonstrated that ant species studied fundamentally distinguished from each other [13, 14, 15, 16, 170, 174]. In
Thus, the forms of social influence of workers on larval diapause are diverse in ants and range from nearly absolute control (in
In many ant species with endogenous- and exogenous-heterodynamic seasonal cycles, the larvae fall into a diapause in the last larval instar. These diapausing larvae continue to feed and to grow slowly and can attain a significantly larger size before overwintering. This larval growth in diapause state is very important for the process of caste differentiation in
9. Evolution of annual cycles of development in ants
Problems of the origin and evolution of the diapause and seasonal cycles of insect development attracted the attention of many researchers (for example, see [175, 176, 177]). The main conclusion reached by most authors is that the evolution of seasonal adaptations occurs largely beyond direct connection with the phylogeny of taxa, and all the elements and parameters of seasonal development known to us, including the diapause itself, the types of cycles, photoperiodic reactions and other regulatory mechanisms, repeatedly, independently and in a variety of ways arise in the evolution of insects. One and the same goal of adapting to certain seasonal environmental conditions can be reached in a variety of ways by combining a whole range of known (or even not yet described) physiological mechanisms [176, 177]. Such a clearly expressed diversity of evolutionary solutions makes it very difficult to analyze the possible ways of the evolution of seasonal development cycles, even within not very large groups of organisms. Nevertheless, some authors proposed various specific sequences of evolutionary events to explain the origin and development of photoperiodic reactions and other physiological mechanisms controlling the diapause and other seasonal adaptations [175]. The most promising approach to the problem of the evolution of seasonal adaptations can be the identification of basic adaptation syndromes, for example, structural types of the annual cycles, diapause forms, ways of synchronizing the cycle with the seasonal rhythm of the climate, etc. Then, it may be productive to look for correlations between all these adaptations and possible ties with the specific environmental conditions in which they are realized and also to analyze the occurrence of the phenomena under study within different taxa.
More and more data appear on the role of diapause in the regulation of the life cycles of insects in tropics. In these regions, the diapause does not always prove to be adapted specifically to the extreme conditions of the abiotic environment, but is often associated with seasonal variations in food availability, migration and reproduction processes. This makes it possible to speak with confidence about the tropical origin of the diapause in many insects [70, 176]. Moreover, the winter hibernation of insects is a relatively recent evolutionary acquisition that arose only after the formation of a glacial climate on the Earth [44]. The available facts do not completely exclude the hypothesis of the possible occurrence of the diapause by the gradual deepening of the developmental delays that first arise exogenously under the direct influence of cold, dryness, lack of food or other unfavorable conditions. The diapause is a fairly simple adaptation from the point of view of the possibility of forming its regulatory hormonal mechanisms, and therefore it could arise in evolution many times and in different ways [176, 177].
Turning to the analysis of the main trends in the evolution of the annual developmental cycles in ants, two most important and closely related questions should be pointed out. First, it is the origin of different forms of diapause, and secondly, possible ways of forming of endogenous-heterodynamic developmental cycles with obligate diapause. It should be borne in mind that the family Formicidae, in its evolutionary origin, is undoubtedly associated with the tropical regions of the Earth, where most of the species of ants live now. From tropical regions, these insects penetrated into zones with temperate climate, forming new species and taxa of higher rank [2, 63]. Another interesting issue, namely the evolution of the structure of the seasonal cycles in ants during their distribution to the north, has been discussed in detail in a special article of V. E. Kipyatkov [88].
It is possible to imagine at least two possible ways of the origin of heterodynamic annual cycles in ants living in temperate and cold climatic zones.
9.1. Subtropical (quasi-heterodynamic) path of evolution
We suppose the possibility of direct adaptation of homodynamic species which penetrate from the tropical regions into subtropics and further into the zone with temperate climate and with cold enough winter. In this case, they do not form a real diapause, and at first acquire the ability to overwinter in the state of a quiescent (cold coma) but suffer from more or less strong mortality, i.e. quasi-heterodynamic seasonal cycles appears. The diapause evolves later and seasonal development becomes exogenously heterodynamic.
The reality of this path of evolution is almost unquestionable. It has been illustrated above by a number of examples of quasi-heterodynamic seasonal cycles, in particular, by the example of two
Probably, quasi-heterodynamic annual cycles with the brood death in late autumn arise in the evolution of many homodynamic ants, which penetrate from tropics into subtropics and further into regions with a warm temperate climate. The nomadic ants
The second real way of verification of our assumption is to study the species taxonomically close to exogenous-heterodynamic ants from the zone with warm temperate climate, but inhabiting subtropics and tropics. The most promising in this respect are the genera
If the onset of a diapause and exogenous-heterodynamic development on the basis of quasi-heterodynamic seasonal cycles seems quite plausible, then the possibility of further evolution in this direction toward the formation of endogenous-heterodynamic cycles with obligate diapause is far from obvious. We do not have at present any definitive evidence of the reality of such an evolution, but in our experiments we found distinct manifestations of endogenous regulation of development in most exogenous-heterodynamic species [144]. The possibilities of evolutionary transition from exogenous- to endogenous-heterodynamic development within the group of closely related species are indirectly confirmed by the following three examples.
Two closely related species of the genus
The second example is a pair of taxonomically related species of the genus
Our observations have shown that
We studied two
9.2. Tropical (preadaptational) path of evolution
Extremely few examples of heterodynamic annual cycles in tropical ants allow us to assume that such species, already possessing diapause (preadaptation), could probably easily penetrate into subtropics and further into the temperate climate zone, using the ability to form a diapause for experiencing a cold winter. The causes for diapause emergence in tropical ants can be diverse. For example, it can be the necessity for survival during the arid or excessively wet seasons of a year, during the periods of shortage or inability to obtain food, etc. It is also possible that the ability to diapause arose as a way of solving internal problems for the colony related to the regulation of development, the processes of caste differentiation and reproduction. Moreover, in tropics, both exogenous and endogenous mechanisms of diapause regulation could be formed, which under the new conditions of a temperate climate, and could be used to synchronize the onset of a diapause with the beginning of a cold season of a year.
Unfortunately, this scheme is almost entirely speculative, first of all, because tropical species with heterodynamic annual cycles have not been investigated experimentally so far, and we know absolutely nothing about the prevalence and nature of diapause in tropical ants. The only argument indirectly confirming the possibility of the tropical origin of heterodynamic annual development in many ants is the rather wide prevalence of endogenous-heterodynamic cycles with obligate diapause among ants inhabiting subtropical and warm temperate climate zone. Among the 39 species of ants from Turkmenistan and the southern coast of the Crimea which we experimentally studied, 18 (46%) are endogenous-heterodynamic. An analysis of a few works, in which at least the simplest laboratory experiments were carried out, allows us to classify as endogenous-heterodynamic four more species from the zone with warm temperate and subtropical climate:
9.3. Taxonomic position and seasonal adaptations
An example of close relationship between taxonomic position and seasonal adaptations is the Formicini tribe. All species studied use the strategy of concentrated brood rearing and are endogenous-heterodynamic with the obligate and very stable diapause of queens and workers and the apparent dominance of endogenous regulatory mechanisms. Probably, such a system of seasonal adaptations evolved already in the ancestors of this tribe.
All studied species of the genus
Other examples relate to fairly definite correlations between taxonomic position and overwintering stages in a number of ants genera. In all species of
Thus, it can be argued that in the evolution of ants, correlations could arise between the nature of seasonal adaptations and the phylogeny of taxa, but no less common are the cases of the absence of such connections, i.e. the appearance of significant differences in the structure and regulation of the annual cycle between related species and, on the contrary, the parallel and independent formation of very similar adaptations in different phylogenetic branches.
10. Conclusions
Most tropical ants demonstrate homodynamic development. They do not exhibit any developmental delays and all-year round the ontogenetic stages from egg to pupa exist in their nests. Some of the quasi-heterodynamic species have permeated into the regions with warm temperate climate but a true diapause did not evolve. In these species, the brood development stops only at temperatures falling below the developmental threshold (consecutive dormancy). So, the ants spend the winter in the state of a quiescent (cold coma), while more or less high mortality rates are observed in their colonies. Most temperate and all boreal climate ants are true heterodynamic. They manifest a true deep winter diapause (prospective dormancy) in their annual cycle.
Heterodynamic ants use two main seasonal strategies with respect to brood rearing. The ants are more likely to follow the strategy of prolonged brood rearing. It is distinguished by the following features: (1) larval diapause is facultative and controlled by environmental (temperature, photoperiod) and social (worker care, queen influence, pheromones, etc.) factors; (2) only some larvae develop from egg to pupa within the same summer season without overwintering (this rapid brood, or summer brood, yields only workers); (3) a large proportion of larvae delay their development, continue to grow in autumn, overwinter in diapause and pupate the next summer (this slow brood, or winter brood, yields both workers and alates).
The strategy of concentrated brood rearing is distinguished by the following features: (1) larvae have no dormancy and complete their development during the summer; (2) the development of all brood stages is thus restricted to the growing season; (3) only queens and workers are able to undergo diapause and overwinter; (4) the colony thus passes the winter without brood. This strategy, however, is not the most common.
The forms of dormancy which were found in ants extend from elementary quiescence to deep diapause. In exogenous-heterodynamic species, the diapause is optional for larvae and queens. The diapause occurs as a result of a direct reaction to temperature decline in the autumn but at a moment when the temperatures still exceed the developmental threshold.
On the contrary in endogenous-heterodynamic ant species, the diapause is compulsory for the colony and occurs eventually under any conditions. Two main factors restrict and control the internal brood-rearing cycle in these species. They are the endogenous timer and environmental conditions, temperature and photoperiod (in some species). But environmental cues can only regulate in some degree the moment of the onset of diapause by accelerating or delaying this event. All cold climate ants have adult diapause, so that their queens and workers are capable for overwintering. Queens and some workers experience diapause several times in their life. On the contrary, the ability of larvae to undergo diapause is not universal in ants. This is a major factor in seasonal cycle evolution in these insects.
The diapause of larvae in ants is facultative in most case. Temperature can affect larval development and induce diapause both directly and through the nurse workers. The larvae appeared to be entirely insensitive to the direct influence of photoperiods. The forms of social impact on larval diapause by workers are diverse in ants and range from nearly absolute control when the physiological state of workers completely defines the fate of larvae, to rather weak effects when in experimental conditions diapausing workers are unable to prevent the development of most overwintered larvae, and spring workers are capable to induce pupation of only a few diapausing autumn larvae.
We can conclude that the similar seasonal adaptations could arise in ant evolution independently many times and usually are not tightly bound to the taxonomic position of species. Nevertheless, several examples of certain seasonal cycle traits clearly confined to specific ant taxa have been found.
Acknowledgments
I am very grateful to students and members of the Department of Entomology, St. Petersburg State University, who participated in these long-term investigations in different years. This work was supported by grants from European Union INTAS program (94-2072), Russian Foundation of Basic Research (97-04-48987, 00-04-49003, 03-04-48854, 06-04-49383), Federal Program “Universities of Russia” (07.01.026, 07.01.327) and the Council for Grants from the President of the Russian Federation and for State Support of Leading Scientific Schools (00-15-97934, 2234.2003.4, 7130.2006.4).
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