Behav. Ecol. Sociobiol. 2, 421-425 (1977) Behavioral Ecology and Sociobiology �9 by Springer-Verlag 1977

How Nepotistic Is the Brain Worm?

David Sloan Wilson*

National Research Institute for Mathematical Sciences, South African Council for Scientific and Industrial Research, P.O. Box 395, Pretoria 0001, Republic of South Africa

Received April 19, 1977

Summary. The evolution of altruism does not necessarily require an extreme amount of kinship. This point is illustrated with an analysis of altruistic behavior in the Trematode parasite Dicrocoelium dendriticum, which apparently can evolve even when the parasites of the host are derived from as many as five different parents.

Introduction

Wickler (1976) stressed that sociobiological concepts can be broadened beyond their usual sphere of vertebrate and social insect behavior, and as an illustration introduced a fine example of altruism in the Trematode parasite Dicrocoelium dendriticum. The life cycle has been worked out by Hohorst and Graefe (1961) and Schneider and Hohorst (1971).

'The adult fluke lives in the bile ducts of the liver of cattle and sheep. Eggs pass from the host with the feces and are eaten by land snails (Zebrina, Helicella). In this first intermediate host, the hatching miracidia develop into mother-sporocysts; these generate daughter-sporocysts and these in turn generate the cercariae larvae. They are emitted by the snail through the respiratory opening, enveloped in a mass of mucus that is produced by the cercariae. Every mucus ball contains several hundred cercariae. They are ingested together with the mucus by ant (Formica) species that nest in open, sunny areas .... Usually about 50 cercariae are taken up by the ant.' (Wickler, 1976, p. 212.)

Once inside the ant, some of the cercariae migrate towards the subesophagal ganglion. The first one to reach it forms a thin-walled cyst and becomes the "brain worm." The rest migrate back into the gaster. The brain worm changes the behavior of the ant, causing it to spend large amounts of time fastened by its mandibles onto

* Present address : Division of Environmental Studies, University of California, Davis, California 95616, USA

422 D.S. Wilson

the tips of grass blades, a location that obviously facilitates being eaten by livestock. However, the brain worm itself has lost the ability to infect its mammal host. In an evolutionary sense, it has sacrificed its reproductive success to increase the probabili ty of the other cercariae within the ant entering the next stage in the life cycle (see the above mentioned authors for more details).

I would like to use the example of the brain worm to clarify a common misconception about altruistic b e h a v i o r - n a m e l y that it requires an extreme amount of kinship to evolve.

For instance, Wickler (p. 212) states that, 'Such altruism can only be favored by selection if there is a high degree of genetic similarity between the brain worm and the cercariae that benefit from its death. In the trematode sporocysts polyembryonic multiplication of one genome takes place, leading to many genetically identical cercariae (James and Bowers, 1967; Szidat, 1962). One need only postulate that the cercariae contained in one mucus ball derive from one sporocyst, that is from one egg of the adult fluke. It seems worthwhile to check this assumption.'

The Model

The following simple calculations indicate that the observed behavior can evolve when the eercariae are derived from as many as five different eggs. Consider a number (T) of parasitized ants (the "trai t -groups" of Wilson's (1977) termi- nology), each of which contains 50 cercariae. There are two types of cercaria, A and B, in proport ions a and b ( = 1 - a). The A-type migrates towards the subesophagal ganglion and the first one to reach it becomes the brain worm. The B-type does not become the brain worm under any circumstances. If it shares an ant with A-types, it benefits from the brain worm without sustaining any cost. However, if it occurs alone in an ant it suffers a decreased probabili ty of being eaten by livestock.

Assume that the cercariae within any ant are derived equally from a number (c) of eggs. In other words, ifc = 5 then the 50 cercariae represent 5 'clutches ' of 10 each originating from 5 original parasite eggs. With random allocation of A and B clutches into ants:

TbC=the expected number of ants containing all B-types. T ( 1 - b C ) = t h e expected number of ants containing 1 or more clutches of A-types.

Let P = t h e probabili ty of an ant being eaten by livestock when it is possessed by a brain worm and P ' = the probabili ty of being eaten while acting normally. In that case the average probabili ty of a cercaria being ingested by livestock (FA, FB) is;

FA -P[5OTa-T(1-b~)] - P [1 (1-b~) -] 50 Ta 50(1 - b)J (1)

v _P(50 rb-50 Tb9 +f '5~ Tbc ( bc ) b c 50Tb =P 1-~- +P'~. (2)

For every ant infected by A-types, a single A-type must sacrifice itself. The rest have a probabili ty P of being ingested by livestock (Eq. (1)). All B-types that occur in ants without A-types have a probabili ty P ' of being ingested by livestock. The rest have a probabili ty of P (Eq. (2)).

How Nepotistic Is the Brain Worm? 423

p~ m P

C=I 1.0

.9

.8

"7

.6

-5

'4

.3

.2

"1

C~ C=21

0 "1 "2 -3 .4 "5 1.0

Q

Fig. 1. The maximum value of P'/P (y-axis) that allows the evolution of altruistic A-type as a function of frequency (a = 1 - b). c, the number of eggs from which the cercariae are derived

The A-type will be selected for it

G > F, (3)

P [ 1 (1-b~) ] (1 bc - ~ - ) + P ' bC 50(1 - b)] > n b- (4)

[ ~ ( 1 - b~) ] bC P 5 0 ( l _ b ) j > P ' ~- (5)

1 b(1 - b c) >P'/P. (6)

50be(1 - b )

Unfortunately we do not know the real value of P'/P and must entertain all possibilities. Figure 1, therefore, shows the maximum value of P'/P that allows the selection of the A-type, for several values of c. When c = 1, ants never contain a mixture of A and B-types, and the brain worm will be selected for if P'/P is 0.98 or less. In other words, the increased probability of being eaten by livestock must compensate for the loss of the brain worm, but no more.

For c > 1 the selection of the A-type is frequency dependent. The shape of the curves make the general conclusions remarkably insensitive to P ' /P, but for convenience assume that the brain worm doubles the probabili ty of the ant being eaten by livestock (P' /P = 0.5). In that case the A-type will be selected to a frequency of 0.96 when the cercariae are derived from two eggs, and to a frequency of 0.45 when the cercariae are derived from five eggs.

424 D.S. Wilson

6, bJ

t.o I

9i

-8

-7

.6

.5

.4

-3

.2

"1

I [ [ I I I I [ I 2 3 4 5 6 ? 8 9 I 0

C Fig. 2. Equilibrium frequencies at P'/P = 0.5 as a function of c. The solid line gives the frequency of the A- type (a) which declines rapidly as the number of clutches increases. The dashed line is the frequency of parasitized ants that contain a brain worm. It remains high

In Figure 2, the equilibrium frequency of A for P' /P = 0.5 is plotted as a function of c (solid line). The dashed line plots the frequency of parasitized ants containing a brain worm at equilibrium ( = l - b e ) . Even though the frequency of A-types declines rapidly, the frequency of brain worms remains high. For instance at c = 5 the equilibrium frequency of A is only 0.45, yet 0.95 of all parasitized ants contain a brain worm. At c = 10, 0.80 of all parasitized ants contain a brain worm. The reason is that the probability of at least one in ten clutches being an A-type is high, even when the A-type is at low frequency.

An analysis has been made for the situation in which c is allowed to vary binomially between ants, but only the results will be reported here. It may be shown that the expected proportion of ants containing only B-types is

Pr (all B-types) = (bp + 1 _p)C#, (7)

where ~ is the average number of clutches per ant and p is chosen such that var c =~(1 -p ) . Furthermore it may be shown that in all cases

(bp + 1 - p)~/" > b c. (8)

In other words a consideration of clutch variation between ants further improves the conditions for the evolution of altruism.

D i s c u s s i o n

These calculations only indicate that the brain worm could have evolved with a relatively high degree of m i x i n g - not that it did. It is quite possible that in nature the ingestion of parasite eggs by snails follows a Poisson distribution, with most

How Nepotistic Is the Brain Worm? 425

snails being infected by a single egg. Furthermore any mechanism promoting the concentration of identical genotypes into mucus balls would certainly be selected for. However, such conditions do not appear to be necessary for the evolution of the trait.

If the parasites within an ant are often derived from more than one clutch, 'selfish' cercariae that do not form brainworms should exist at some equilibrium frequency in the population. Because most of the parameters in the model (costs and benefits of altruism, size and variation of parasite 'trait-groups') are measurable, the brain worm might then be a fertile testing ground for sociobiologi- cal concepts.

To summarize, the evolution of altruism does not necessarily require a high degree of kinship. Of course this can only strengthen Wickler's main argument. In addition to applying sociobiological concepts to new taxa, we should also apply them to new situations of 'diluted kin groups', in which highly directed interactions among relatives are not apparent. See Wilson (1977) for a more thorough discussion of the concepts.

Acknowledgements. I am grateful to A.B. Clark for helpful discussion and T.J. Stewart for the analysis of clutch variation between ants. An anonymous reviewer provided several valuable suggestions.

References

Hohorst, W., Graefe, G.: Ameisen - obligatorische Zwischenwirte des Lanzettegels (Dicrocoelium dentriticum). Naturwissenschaften 48, 229-230 (1961)

James, B.L., Bowers, E.A.: Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimaena. Parasitology 57, 602625 (1967)

Schneider, G., Hohorst, W.: Wanderung der Metacercarien des Lanzett-Egels in Ameisen. Natur- wissenschaften 58, 327-328 (1971)

Szidat, L.: Uber eine ungew~Shnliche Form parthenogenetischer Vermehrung bei Metacercarien einer Gymnopallus-Art aus Myrilus platensis, Gymnopallus australis n. sp. des Siidatlantik. Z. Parasitenk. 22,196-213 (1962)

Wickler, W.: Evolution-oriented ethology, kin selection, and altruistic parasites. Z. Tierpsychol. 42, 205514 (1976)

Wilson, D.S.: Structured demes and the evolution of group-advantageous traits. Amer. Nat. 111, 157- 185 (1977)