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Testing parent-offspring conflicts in insect parasitoids
12 ./increase fimess lr\ judenib mi do so al the exilenst? of Thereby redi:cinq Ihe nu’ E.,ffspring their parents can This pits seiecllon for raits agains: selection for ,adults to produce large )I of offspring. Trivers defin@d p -1ffsprirg conflicis as situatkn$;,
”
. widely discussed2, few studies to docuin natijre. This is Few conclusive experi: -‘meF t3. Such an experito show (I) that i6#
:_darious para_ases3f a solitary linw
eaaj
of the
iidae) in their host caterpil&&$%jts;emc)rged frpm this par&* Phntnn h,, E&L rz:rPrmP
.
TREE vol. 2, no. 8, August
Insect parasitoids attack the egg, larval or pupal stages of their insect hosts either by attaching eggs to the outside or by injecting eggs into the host. The morphology of the subsequent parasitic larvae divides parasitoids into two groups: solitary and gregarious. The larvae of solitary species typically have mandibles which they use to kill any other larvae on a host. Consequently, even if more than one egg is laid on a host, only one larva survives to adulthood. In contrast, the larvae of gregarious species lack mandibles, and several can survive on a single host. Examples of solitary and gregarious parasitic wasps are given in Fig. 1. A parent-offspring conflict arises when a female would benefit from laying several gregarious larvae, but selection on larvae favors fighting, and siblicide reduces the number of survivors per host to one. The opposition between selection on parents and selection on offspring is best explained by first considering a 232
gregarious parasitoid species in which only one female oviposits per host. As a female lays more eggs, the survivorship of the resulting larvae decreases as they compete for the limited food provided by a host. When very large numbers of eggs are laid, larval competition becomes so severe that the total number of offspring surviving from a host decreases. Therefore, at some intermediate value there is an optimal clutch size that gives the maximum number of offspring surviving per host. Among different species of optimal clutch sizes parasitoids, range from one to several hundred. To examine selective forces on offspring, assume an allele for fighting larvae arises in a population of gregarious parasitoids. Here, it will be assumed that the fighting allele is dominant, although a similar argument holds for recessive alleles. Larvae carrying the fighting allele will be free from competition with siblings for food, and this will help the introduced fighting allele to spread in the population. However, fighting larvae run the risk of being killed by siblings, who are also likely to be fighters because they are genetically related. In effect, this means that copies of the fighting allele will destroy each other, making the spread of the allele more difficult. Whether the advantage of escaping competition outweighs the disadvantage of fighting larva killing each other depends both on the severity of competition and the number of eggs laid by a female per host. If females lay large numbers of eggs, the probability that any one fighting larva survives combat with its many fighting siblings is low. Godfray shows that the advantages for the fighting allele outweigh the disadvantages whenever the clutch size is below about four. Therefore, species of gregarious parasitoids which attack small hosts, and consequently have small clutch sizes, are likely to be converted into solitary parasitoids. Box 1 gives this result in more detail. For populations in which the fighting allele is fixed, the offspring control the parent-offspring conflict. This exacts a cost from the parents: the reduced number of offspring produced per host. When the clutch sizes of a gregarious parasitoid are small enough for a fighting allele to invade, females suffer only a small loss, because the potential number of offspring a female could produce per host is small. However, after the fighting allele is fixed, the cost to the parents of the parent-offspring conflict can be much greater. This is
1987
because it is difficult for a solitary parasitoid with fighting larvae to revert to being gregarious. Godfray shows that a dominant invade a allele can gregarious population of solitary parasitoids only when (1) females occasionally lay more than one egg per host, and (2) gregarious siblings, if they occur together in the same host, each have greater fitness than the fighting larvae occurring alone. This requires hosts to be very large, so that the two gregarious larvae do not have to compete for food within the host. The difficulty of a gregarious allele invading a population of solitary parasitoids makes fighting larvae an evolutionary sink. Therefore, a solitary parasitoid with fighting larvae might attack a host capable of supporting a large number of gregarious larvae. The resulting costs of the parent-offspring conflict to the parents are correspondingly large. Godfray’s model predicts several patterns that should be seen in nature, and le MasurieP has provided evidence to support these predictions for the genus Apanteles (Braconidae), a large genus of parasitic wasps that includes both solitary and gregarious species. First, small hosts relative to the size of the parasitoid are victimized primarily by solitary species. Gregarious Apanteles which lay 2-11 eggs per host are rare, possibly because these species would be susceptible to conversion to solitary habits. Second, both solitary and gregarious species parasitize hosts of intermediate size, even though the solitary species are not larger than the gregarious species. This could be explained if the evolutionary ancestor of these solitary species parasitized small hosts and consequently had solitary, fighting larvae. As species within the phylogenetic line adopted larger hosts, the character for fighting larvae would have been conserved. Although these observed patterns give indirect support for Godfray’s model, the most exciting thing about the model is that it can be tested directly. Strand and Waage are currently developing experiments to do this, using the gypsy moth parasitoids Brach ymeria intermedia (Hymenoptera: Chalcididae). These parasitic wasps are typical solitary species, with mandibulate larvae fighting to the death within hosts. However, if adult females are treated with small quantities of diflubenzuron, a chitin synthesis inhibitor, the eggs they lay will give rise to larvae with reduced mandibles that do not aggressively attack other larvae7. This manipulation of
TREE vol. 2, no. 8, August
1987
females gives control of the parentoffspring conflict to the parents. It is then possible to calculate the number of larvae that could survive per host in the absence of siblicide, and this will reveal the cost to the parents of reduced reproductive output when their offspring kill each other. This experiment will give the first direct demonstration of parentoffspring conflicts by measuring the costs of the conflict in terms of lifetime fitness. It also leads to a tantalizing question: if such a chem-
Population biology is underpinned by a rich and sophisticated body of mathematical theory that not everybody finds either useful or interesting. Recently, for example, Andrewartha and Birch’ wrote in The Ecological Web: ‘Unfortunately, there is a powerful trend toward excessively abstract mathematical models in the modern literature on population . . We cannot see many ecology testable hypotheses emerging from such abstract models, despite the claim that [they] can be useful in suggesting interesting experiments or data gathering enterprises’. Recent work by Murdoch and McCauley2,3 shows that such pessimism is very wide of the mark. They studied populations of Daphnia (water fleas) and their algal food supply to provide an important test of one of the central assumptions of mathematical population biology. Natural populations exhibit a dynamic fascinating range of behaviours4. Some are constant; some fluctuate apparently randomly over small or large amplitudes; and still others appear to cycle in a regular manner. There are two ways of reproducing this range of behaviour in mathematical models. The first is to vary the structure of the model. For example, an insect host-parasitoid model in NicholsonBailey form, in which a randomly distributed host population grows exponentially unless checked by randomly searching parasitoids. is wildly unstables. This behaviour is transformed by making structural alterations to the model, for example by incorporating host refuges, or by assuming that host populations experience some self-limitation on their growths. Alternatively, adding extra species (in the form of a com-
John Lawton is at the Dept of Biology, University of York, York YOl 5DD,UK.
ical exists, why are there no solitary parasitoids in which females enforce gregariousness on their offspring? Or maybe there are. Acknowledgements I thank Mike Strand for letting me in on his work and allowing me to discuss it in this article. Erick Greene generously provided help with the manuscript and the photographs in Fig. 1.
2 Parker, G.A. and Macnair, M.R. (1978) Anim. Behav. 26,79-96 3 Stamps, J., Clark, A., Arrowood, P. and Kus, B. (1985) Behaviour94, l-40 4 Trivers, R.L. and Hare, M. (19761 Science i 91,249-263 5 Godfray, H.C.J. (1986)Am. Nat. 129, 221-233 6 le Masurier, A.D. fcol. Entomol. (in press) 7 Khoo, B.K., Forgash, A.J., Respicio, N.C. and Ramaswamy, S.B. (1985) Envir. Entomol. 14,820-825
References 1 Trivers, 249-264
Anthony Ives is at the Dept of Biology, Princeton University, Princeton, NJ 08544, USA.
R.L. (1974) Am. Zoo/. 14,
DaphrziaPopulation Dynamics in
Theory andPractice John H. Lawton peting host population, or a second species of parasitoid) also changes the structure of the model, and not alters usually the surprisingly dynamics (e.g. Ref. 6). model behaviour Alternatively, can be changed by holding structure constant, and varying parameter values. Thus refuges may or may not stabilize enemy-victim interactions, depending upon the proportion (or number) of victims able to gain access to the refuge5,7. One of the simplest demonstrations of the way in which dynamic behaviour changes as parameter values change in a structurally constant model is provided by the time-lagged logistic, describing the single species growth of a population8. The equation is: dNldt
= r/V [I-N(t-T)/
Kl
(1)
where N is population density at time t, r is population rate of increase, K is the equilibrium population size, and T is a time lag in the response of the population to density. Without changing the structure in any way, this model can generate either a stable population (for 0 < rT < e-l), or damped oscillations when e--l < rT < ~r/2. Stable limit cycles are generated when rT > 7~12. Even the most sceptical field naturalist would probably concede that structural changes to species interactions are likely to alter population behaviour. But what evidence is there that simply altering parameter values under structurally similar conditions changes the behaviour of field populations? Without such evidence, much of theoretical mathematical ecology might be elegant,
but wrong! To date, different population behaviours have been sought among biologically disparate taxa and food webs (e.g. Ref. 9). They have not been demonstrated in the field for one species, or a closely related set of species, under conditions that appear to rule out structural changes. As Murdoch and McCauley point out2z3, simple algalherbivore food chains made up of Daphnia and their phytoplankton prey seem ideal subjects for such a test. Gathering together published data from laboratory and field systems, together with their own semi-natural experiments in farm stock-tanks at the University of California in Santa Barbara, they discovered3 three distinct classes of Daphnia-algal population behaviour under structurally identical conditions. The simplest dynamics, class 1, were and algal popustable Daphnia lations, observed in six examples. Class 2 dynamics were apparently stable limit cycles between Daphnia and algae, with the Daphnia lagging behind the algae, as expected in classical prey-predator dynamics; 15 populations cycled in this way. Finally, they found four examples of stable algae but cyclic Daphnia (class 3 dynamics). It could, of course, be argued that because the study embraces different species of both algae and Daphnia, as well as different numbers of algal species, the crucial assumption of structural constancy is violated, or at best not proven. But as McCauley and Murdoch point out3, Daphnia pulicaria in Lake Washington exhibited all three classes of behaviour 233
”
. widely discussed2, few studies to docuin natijre. This is Few conclusive experi: -‘meF t3. Such an experito show (I) that i6#
:_darious para_ases3f a solitary linw
eaaj
of the
iidae) in their host caterpil&&$%jts;emc)rged frpm this par&* Phntnn h,, E&L rz:rPrmP
.
TREE vol. 2, no. 8, August
Insect parasitoids attack the egg, larval or pupal stages of their insect hosts either by attaching eggs to the outside or by injecting eggs into the host. The morphology of the subsequent parasitic larvae divides parasitoids into two groups: solitary and gregarious. The larvae of solitary species typically have mandibles which they use to kill any other larvae on a host. Consequently, even if more than one egg is laid on a host, only one larva survives to adulthood. In contrast, the larvae of gregarious species lack mandibles, and several can survive on a single host. Examples of solitary and gregarious parasitic wasps are given in Fig. 1. A parent-offspring conflict arises when a female would benefit from laying several gregarious larvae, but selection on larvae favors fighting, and siblicide reduces the number of survivors per host to one. The opposition between selection on parents and selection on offspring is best explained by first considering a 232
gregarious parasitoid species in which only one female oviposits per host. As a female lays more eggs, the survivorship of the resulting larvae decreases as they compete for the limited food provided by a host. When very large numbers of eggs are laid, larval competition becomes so severe that the total number of offspring surviving from a host decreases. Therefore, at some intermediate value there is an optimal clutch size that gives the maximum number of offspring surviving per host. Among different species of optimal clutch sizes parasitoids, range from one to several hundred. To examine selective forces on offspring, assume an allele for fighting larvae arises in a population of gregarious parasitoids. Here, it will be assumed that the fighting allele is dominant, although a similar argument holds for recessive alleles. Larvae carrying the fighting allele will be free from competition with siblings for food, and this will help the introduced fighting allele to spread in the population. However, fighting larvae run the risk of being killed by siblings, who are also likely to be fighters because they are genetically related. In effect, this means that copies of the fighting allele will destroy each other, making the spread of the allele more difficult. Whether the advantage of escaping competition outweighs the disadvantage of fighting larva killing each other depends both on the severity of competition and the number of eggs laid by a female per host. If females lay large numbers of eggs, the probability that any one fighting larva survives combat with its many fighting siblings is low. Godfray shows that the advantages for the fighting allele outweigh the disadvantages whenever the clutch size is below about four. Therefore, species of gregarious parasitoids which attack small hosts, and consequently have small clutch sizes, are likely to be converted into solitary parasitoids. Box 1 gives this result in more detail. For populations in which the fighting allele is fixed, the offspring control the parent-offspring conflict. This exacts a cost from the parents: the reduced number of offspring produced per host. When the clutch sizes of a gregarious parasitoid are small enough for a fighting allele to invade, females suffer only a small loss, because the potential number of offspring a female could produce per host is small. However, after the fighting allele is fixed, the cost to the parents of the parent-offspring conflict can be much greater. This is
1987
because it is difficult for a solitary parasitoid with fighting larvae to revert to being gregarious. Godfray shows that a dominant invade a allele can gregarious population of solitary parasitoids only when (1) females occasionally lay more than one egg per host, and (2) gregarious siblings, if they occur together in the same host, each have greater fitness than the fighting larvae occurring alone. This requires hosts to be very large, so that the two gregarious larvae do not have to compete for food within the host. The difficulty of a gregarious allele invading a population of solitary parasitoids makes fighting larvae an evolutionary sink. Therefore, a solitary parasitoid with fighting larvae might attack a host capable of supporting a large number of gregarious larvae. The resulting costs of the parent-offspring conflict to the parents are correspondingly large. Godfray’s model predicts several patterns that should be seen in nature, and le MasurieP has provided evidence to support these predictions for the genus Apanteles (Braconidae), a large genus of parasitic wasps that includes both solitary and gregarious species. First, small hosts relative to the size of the parasitoid are victimized primarily by solitary species. Gregarious Apanteles which lay 2-11 eggs per host are rare, possibly because these species would be susceptible to conversion to solitary habits. Second, both solitary and gregarious species parasitize hosts of intermediate size, even though the solitary species are not larger than the gregarious species. This could be explained if the evolutionary ancestor of these solitary species parasitized small hosts and consequently had solitary, fighting larvae. As species within the phylogenetic line adopted larger hosts, the character for fighting larvae would have been conserved. Although these observed patterns give indirect support for Godfray’s model, the most exciting thing about the model is that it can be tested directly. Strand and Waage are currently developing experiments to do this, using the gypsy moth parasitoids Brach ymeria intermedia (Hymenoptera: Chalcididae). These parasitic wasps are typical solitary species, with mandibulate larvae fighting to the death within hosts. However, if adult females are treated with small quantities of diflubenzuron, a chitin synthesis inhibitor, the eggs they lay will give rise to larvae with reduced mandibles that do not aggressively attack other larvae7. This manipulation of
TREE vol. 2, no. 8, August
1987
females gives control of the parentoffspring conflict to the parents. It is then possible to calculate the number of larvae that could survive per host in the absence of siblicide, and this will reveal the cost to the parents of reduced reproductive output when their offspring kill each other. This experiment will give the first direct demonstration of parentoffspring conflicts by measuring the costs of the conflict in terms of lifetime fitness. It also leads to a tantalizing question: if such a chem-
Population biology is underpinned by a rich and sophisticated body of mathematical theory that not everybody finds either useful or interesting. Recently, for example, Andrewartha and Birch’ wrote in The Ecological Web: ‘Unfortunately, there is a powerful trend toward excessively abstract mathematical models in the modern literature on population . . We cannot see many ecology testable hypotheses emerging from such abstract models, despite the claim that [they] can be useful in suggesting interesting experiments or data gathering enterprises’. Recent work by Murdoch and McCauley2,3 shows that such pessimism is very wide of the mark. They studied populations of Daphnia (water fleas) and their algal food supply to provide an important test of one of the central assumptions of mathematical population biology. Natural populations exhibit a dynamic fascinating range of behaviours4. Some are constant; some fluctuate apparently randomly over small or large amplitudes; and still others appear to cycle in a regular manner. There are two ways of reproducing this range of behaviour in mathematical models. The first is to vary the structure of the model. For example, an insect host-parasitoid model in NicholsonBailey form, in which a randomly distributed host population grows exponentially unless checked by randomly searching parasitoids. is wildly unstables. This behaviour is transformed by making structural alterations to the model, for example by incorporating host refuges, or by assuming that host populations experience some self-limitation on their growths. Alternatively, adding extra species (in the form of a com-
John Lawton is at the Dept of Biology, University of York, York YOl 5DD,UK.
ical exists, why are there no solitary parasitoids in which females enforce gregariousness on their offspring? Or maybe there are. Acknowledgements I thank Mike Strand for letting me in on his work and allowing me to discuss it in this article. Erick Greene generously provided help with the manuscript and the photographs in Fig. 1.
2 Parker, G.A. and Macnair, M.R. (1978) Anim. Behav. 26,79-96 3 Stamps, J., Clark, A., Arrowood, P. and Kus, B. (1985) Behaviour94, l-40 4 Trivers, R.L. and Hare, M. (19761 Science i 91,249-263 5 Godfray, H.C.J. (1986)Am. Nat. 129, 221-233 6 le Masurier, A.D. fcol. Entomol. (in press) 7 Khoo, B.K., Forgash, A.J., Respicio, N.C. and Ramaswamy, S.B. (1985) Envir. Entomol. 14,820-825
References 1 Trivers, 249-264
Anthony Ives is at the Dept of Biology, Princeton University, Princeton, NJ 08544, USA.
R.L. (1974) Am. Zoo/. 14,
DaphrziaPopulation Dynamics in
Theory andPractice John H. Lawton peting host population, or a second species of parasitoid) also changes the structure of the model, and not alters usually the surprisingly dynamics (e.g. Ref. 6). model behaviour Alternatively, can be changed by holding structure constant, and varying parameter values. Thus refuges may or may not stabilize enemy-victim interactions, depending upon the proportion (or number) of victims able to gain access to the refuge5,7. One of the simplest demonstrations of the way in which dynamic behaviour changes as parameter values change in a structurally constant model is provided by the time-lagged logistic, describing the single species growth of a population8. The equation is: dNldt
= r/V [I-N(t-T)/
Kl
(1)
where N is population density at time t, r is population rate of increase, K is the equilibrium population size, and T is a time lag in the response of the population to density. Without changing the structure in any way, this model can generate either a stable population (for 0 < rT < e-l), or damped oscillations when e--l < rT < ~r/2. Stable limit cycles are generated when rT > 7~12. Even the most sceptical field naturalist would probably concede that structural changes to species interactions are likely to alter population behaviour. But what evidence is there that simply altering parameter values under structurally similar conditions changes the behaviour of field populations? Without such evidence, much of theoretical mathematical ecology might be elegant,
but wrong! To date, different population behaviours have been sought among biologically disparate taxa and food webs (e.g. Ref. 9). They have not been demonstrated in the field for one species, or a closely related set of species, under conditions that appear to rule out structural changes. As Murdoch and McCauley point out2z3, simple algalherbivore food chains made up of Daphnia and their phytoplankton prey seem ideal subjects for such a test. Gathering together published data from laboratory and field systems, together with their own semi-natural experiments in farm stock-tanks at the University of California in Santa Barbara, they discovered3 three distinct classes of Daphnia-algal population behaviour under structurally identical conditions. The simplest dynamics, class 1, were and algal popustable Daphnia lations, observed in six examples. Class 2 dynamics were apparently stable limit cycles between Daphnia and algae, with the Daphnia lagging behind the algae, as expected in classical prey-predator dynamics; 15 populations cycled in this way. Finally, they found four examples of stable algae but cyclic Daphnia (class 3 dynamics). It could, of course, be argued that because the study embraces different species of both algae and Daphnia, as well as different numbers of algal species, the crucial assumption of structural constancy is violated, or at best not proven. But as McCauley and Murdoch point out3, Daphnia pulicaria in Lake Washington exhibited all three classes of behaviour 233