J. Theoret. Biol.

(1966) 11, 54-58

The Advantages of Hermaphroditism and Parthenogenesis

J. TOMLINSON

San Francisco State College Biology Dcparrmulr.

San Francisco, Califorttia, U.S..4 _

(Received 30 November 1964, and i/l rcvised,fbrw 16 August 1965)

Poisson data on the probability of successful fertilization contact by

gonochoristic, hermaphroditic, and parthenogenetic species indicate that
the latter sexual types have an increasing advantage as populations
become sparse, when the populations are thinly scattered in temporary
or marginal habitats, and when the effective breeding area is reduced by
lack of motility as in sessile or sluggish animals without widely distributed
gametes.

One way to estimate the advantages of a given type of reproductive mecha-

nism is to determine how it effects the relative chances of the individuals
getting together and of successfully producing offspring as a result of meeting.
The advantages of these reproductive mechanisms may be analyzed mathe-
matically, using the probabilities of the Poisson distribution. When the
propagule is small the advantages of being abIe to reproduce without hunting
a mate of the opposite sex would be important. The probability of successfully
establishing a colony of gonochoristic animals (with separate sexes) has
been presented by MacArthur & Wilson (1963).
We can see, of course, that self-fertilizing hermaphrodites and partheno-
genetic individuals will not need to get together with another of their kind
at all, and hence, for the purpose of this discussion, we will treat partheno-
genesis the same as self-fertilizing hermaphroditism. We will be considering
the “effective breeding area” of an organism, which is the area successfully
served by a breeding individual. This area is a function of the mobility of
the contacting units, including the adults and ultimately the gametes.
The mobility of sperm moved by water action is as effective in transporting
the male function in breeding as a mobile male would be. Thus, organisms
that discharge sperm into the sea in large numbers would be considered
mobile in this argument. Although most hermaphrodites are sessile or
sluggish, there are a few hermaphrodites with apparently mobile gametes,
e.g. the tunicates and protandric pelecypods. The Chaetognatha are striking
exceptions in being hermaphroditic and highly mobile, although it is thought
 HERMAPHRODITISM AND PARTHENOGENESIS 55

that they arose from sluggish, bottom-dwelling ancestors. One must also
consider those cases in which mobility is linked with the gonochoristic
portion of the sexual cycle. The best example of this is the well-known
aphid. Here the gonochoristic stages are winged and therefore highly mobile,
while the parthenogenetic stages are wingless.
We will return to the problem of mobility after we look at the results of
the mathematical study. The results are shown in Figs 1 and 2. Figure 1

Average no. of orgon~sms withm the effectwe breeding Oreo

FIG. 1. FIG. 2.

FIQ. 1. The probability of at least one successful breeding contact, as a function of the
average number of organisms within the effective breeding area.
FIG. 2. The relative probability of at least one successful breeding contact, as a function
of the average number of organisms within the effective breeding area. Selfers - self-
fertilizing hermaphroditic or parthenogenetic organisms; non-selfers - non-self-fertilizing
hermaphroditic organisms; gonochoristic = species whose sexes are in separate organisms.
56 J. TOMLINSON

plots the probability of at least one successful gametic contact between

individuals capable of breeding, as a function of the average number ot
organisms within the effective breeding area. It is obvious that a self-fertilizing
hermaphroditic or parthenogenetic individual will always be certain of a
successful contact with a reproductively capable individual, namely itself.
Therefore the probability of at least one successful contact is 1,O, or a cer-
tainty, for these forms at a// densities. In considering non-selhng hermaphro-
dites, the probability of encountering another individual can be determined
from the Poisson distribution, and, being hermaphroditic, this contact will
always be successful, i.e. the other individual will be of the right sex.
In gonochoristic species, the probability of contacting another individual
is still a function of population density, but now a correction must be
imposed to calculate the probability of a contact with at least one of the
opposite SP.Y.The formulae for extracting these figures from tables of Poisson
distribution are given in Fig. 1, assuming an equal sex ratio.
In Fig. 2, we can compare the relative probability of a successful encounter
among the three sexual types (i.e. gonochoristic, hermaphroditic and
parthenogenetic). This can be interpreted for each curve as the advantage
of the reproductive method on the top of the label for the curve. over the
method on the bottom of the label.
Let us see why such a theoretical advantage goes to hermaphroditic and
parthenogenetic forms. It can easily be seen that if the chance of encountering
another animal is extremely small, it is highly advantageous to have that rare
individual of a type that would insure fertilizing capability. In hermaphrodites
this rarely-encountered individual will ahc.u~s have fertilizing capabilities,
while the gonochoristic individual’s chances are one-half (assuming an
equal sex ratio). Therefore, the chances of at least one successful contact
favors the hermaphrodite by a factor of at least two. As the population
becomes very dense, there is a high probability that an animal will encounter
another with fertilizing capability, so there is essentially no advantage in
being hermaphroditic. Intermediate values of density and breeding area
show a marked decrease in the advantages of hermaphroditism and
parthenogenesis with an increase in density, such that the adaptive value
of hermaphroditism would be most strongly expressed when populations
are very sparse. This advantage could be appreciated for early colonizers
and for those species which tend to be distributed by chance in small
numbers.
It will be noted that the advantage of hermaphroditism and partheno-
genesis drops to very low values with access on the average to only seven
to eight other animals (of either sex). Thus, these traits would seem to be
especially favorable to sessile and sluggish animals, or to animals such as
 HERMAPHRODITISM AND PARTHENOGENESIS 57

snails who are dispersed by such means as on the feet of birds to temporary
ponds where the chance of encountering another individual is small. By the
time populations have built up to respectable densities, hermaphroditism
and parthenogenesis are no longer of any advantage in this regard.
Insofar as mobility affects the effective breeding area of an individual, to
that extent mobility is less important to hermaphrodites than to gonochoristic
animals. As the density approaches zero, mobility in extending the breeding
area is twice as important to a gonochoristic animal as it is to a non-selfing
hermaphrodite, and infinitely more important in either than it is to a self-
fertilizing hermaphroditic or parthenogenetic individual. Thus, many
hermaphroditic and parthenogenetic animals can afford to be sessile or
sluggish. Expressed in another way, the only animals that are adapted to
exist in the relative isolation of small temporary pools (unless they have
resistant eggs or other stages) or in small numbers, either free living or as
parasites, are hermaphroditic or parthenogenetic species. As an example,
tapeworms are hermaphroditic, with self-fertilizing potential, while the
relatively more numerous and motile blood flukes are gonochoristic. In
similar generalities, gastropods are largely hermaphroditic while cephalopods
are gonochoristic; oligochaetes are hermaphroditic while polychaetes are
usually gonochoristic.
When we consider the distribution of parthenogenetic races or species,
we almost always find that the parthenogenetic forms have a much wider
geographic range than the gonochoristic ones. White (1954) states that
perhaps the parthenogenetic forms have found it easier to expand their
range just because every individual was capable of founding a local colony of
the species, and because there was no “reproductive wastage” however small
the population or scattered the individuals. This is amplified and quantified
in Fig. 2, showing that parthenogenesis, as with selfing hermaphroditism,
is extremely useful where the population densities are thin, namely at the
edges of the species or racial distribution.
Evidence that the advantages of parthenogenesis are utilized in nature
is reviewed by Suomalainen (1962) and is given by White (1954) and Stalker
(1956) for the species or races of the well-known arthropod genera Saga
(orthopteran), Solenobia (lepidopteran), Trichoniscus (isopod), and Drosophila
(dipteran). In general these parthenogenetic groups have widely scattered,
discontinuous populations in very precarious habitats. The advantage in a
marginal distribution of an initially small, disjunct population goes to the
parthenogenetic forms.
It will be noted, however, that few organisms are strict selfers or partheno-
gens. This is probably due to the fact that although there is an improved
chance of gametic union, gene how between portions of the population is
58 J. TOMLINSON

completely eliminated. There are many non-selfing hermaphrodites, whose

gene flow is not restricted. The production of a single type of gamete in each
sex of a gonochoristic species relative to the more complex and thus con-
ceivably more troublesome production of two types of gametes in hermaphro-
dites may be responsible for the predominance of gonochorism in animals.
Many articles in the literature indicate that hermaphroditism or partheno-
genesis recurs frequently in gonochoristic species (Peacock & Weidmann,
1964; Suomalainen, 1962; White, 1954). Although some of these isolated
cases are gynandromorphs or pathological anomalies, the incidence in many
forms is sufficiently high to assure the availability of these sexual types when
situations such as small disjunct populations persist.

I would like to thank F. F. Sheehan of our Mathematics Department for his

valuable assistance. This investigation was supported in whole by Public Health
Service Research Grant GM-09953 from the National Institutes of Health.

REFERENCES
MACARTHUR, R. H. & WILSON, E. 0. (1963). Evolution, N. Y. 17 (4), 373.
PEACOCK, A. D. & WEIDMANN, U. (1964). Przegl. 2001. 8 Cl), 16.
STALKER, H. D. (1956). Evolution, N. Y. 10(4), 345.
SUOMALAINEN, E. (1962). A. Rev. EM. 7, 349.
WHITE, M. J. D. (1954).“Animal Cytology and Evolution” (2nd ed.), 454 pp. Cambridge :
Cambridge University Press.