A Hipótese Da Vantagem Do Tamanho

The Evolution of Hermaphroditism Among Animals
Author(s): Michael T. Ghiselin

Reviewed work(s):
Source: The Quarterly Review of Biology, Vol. 44, No. 2 (Jun., 1969), pp. 189-208
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2819439 .
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THE EVOLUTION OF HERMAPHRODITISM
AMONG ANIMALS
BY MICHAEL T. GHISELIN
Department of Zoology, University of California,Berkeley, California 94720
ABSTRACT
Possible selective advantages, including some new ones, for hermaphroditism are
reviewed. It is proposed that hermaphroditism should evolve under the following condi-
tions: (a) where it is hard to find a mate; (b) where one sex benefits from being larger
or smaller than the other; or (c) where there are small, genetically isolated populations.
Some conceptual problems and a comparative means of study are discussed. The litera-
ture is reviewed to show the conditions under which hermaphroditism may have
evolved. It is concluded that all three explanations have some validity.
INTRODUCTION We may also dismiss the Lamarckian notion

that the mere condition of sessility disturbs
LTHOUGH HERMAPHRODITISM metabolism and somehow brings about the her-
has been known to science since maphroditic condition (G. Smith, 1908). Such
antiquity, its functional signifi- views, very popular a few decades ago, have
cance is only partly understood yet to disappear entirely from the physiological
~~~~(Mayr, 1963; p. 406). Pre- literature. Also needing no further refutation
Darwinian workers seem largely to have taken is the old idea that ancestral metazoans were
it for granted that sex is "for" reproduction, hermaphroditic, and that the sexes became
and that uniting the sexes in a single individ- separated during progression from "lower" to
ual would dispense with the need for a mate. "higher" forms. Such notions are not just the
Such views in part reflect the very gradual result of faulty scientific reasoning: the facts
development of the study of sexual reproduc- show that the change has gone in both direc-
tion. Yet they also retain a measure of truth, tions. Even if there is a general tendency
for many plants, and some animals, are her- toward division of labor between the sexes
maphrodites specially adapted to permit self- (Haeckel, 1874; Muller, 1932; Altenberg, 1934),
fertilization. The necessity to reproduce at all it is still not possible to explain particular
costs should favor the development of selfing instances of the shift from the hermaphroditic
wherever the environment is such that the state to separation of sexes, or vice versa.
transfer of gametes between individuals is
hindered. It appears that selfing has originated MODELS
convergently in adaptation to special condi-
tions, for it is often facultative. Even There are at least three possible explana-
though selfing is quite detrimental on the tions of the origin of hermaphroditism which
whole, it is more advantageous to self-fertilize do seem consistent with modern biological
than not to reproduce at all (Darwin, 1876). thinking. After these hypotheses are proposed,
There is also the difficulty of separating the a means of testing them will be discussed,
original function from the present one; her- followed by a survey of hermaphroditism
maphroditism might predispose an organism throughout the animal kingdom, in which the
to selfing, but this does not tell us why the evidence bearing on each hypothesis will be
sexes became united in the first place. evaluated.
189

190 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 44
Low Density Model Size Advantage Model
The first hypothesis is the classical explana- The second hypothesis, or size advantage
tion of hermaphroditism in terms of selection model, accounts for some of the known in-
theory. Termed the low density model, it dates stances of sequential hermaphroditism. Sup-
from the last century (e.g., Meyer, 1888) and pose that the reproductive functions of one
seems to have been implicit in Darwin's mono- sex were better discharged by a small animal,
graph on barnacles (Darwin, 1851, 1854). It or those of the other sex by a large one. An
has lately been treated mathematically by Tom- animal which, as it grew, assumed the sex ad-
linson (1966). In an animal having any attri- vantageous to its current size would thereby
bute that reduces the opportunities for mating increase its reproductive potential. The model
(such as low motility or low population den- could be extended to cover other advantages
sity), the probability will be high that the other of membership in a particular sex at a given
members of its species which it encounters will period of life, independent of size as such
not be of the opposite sex. Hermaphrodites (C. L. Smith, 1967). Consider the implications
have no such problem. There are other adap- of the facts that eggs are generally larger than
tations which could (and do) evolve in response sperm, and that there is a distinct lower limit to
to the same selective influence (Mosimann, the size of an egg. The larger the female, the
1958). Among these are parthenogenesis and greater the number of eggs that could be pro-
self-fertilization (Suomolainen, 1950, 1962; duced (the actual relationship is not a simple
White, 1954). Although these adaptations have one-Sprules, 1967). In benthic marine in-
some disadvantages, they certainly could be vertebrates with a free-swimming larval stage,
favored by selection in some organisms. An- an individual that happened to reach, without
other possibility is vegetative reproduction, much delay, a suitable spot for post-larval
which (perhaps for this reason) is so prominent development, could grow rapidly and be ready
in sessile animals and in plants. Still another to function as a female, with greater reproduc-
variation is a close (even permanent) association tive potential than later, smaller arrivals. An
between members of the two sexes, such as individual delayed in finding a suitable locality
occurs in deep-sea angler fishes with dwarf could still reproduce when small, but could
males. Phenomena of the "dwarf male" type do so better if male than female. The inverse
occur side by side with hermaphroditism in relationship, proterogyny, might occur where
cirripedes, even within a single species. The it is advantageous for a male to be large-for
frequency of hermaphroditism in plants has example, where there is sexual selection, or
been attributed to their sessility (East and where the male cares for the young. Efforts to
Jones, 1919; Mather, 1940; Lewis, 1942), and explain protandry and proterogyny will suc-
numerous attempts to apply versions of the ceed, for all instances, only if something more
low density model have been made. Stalker than a size advantage is invoked.
(1956) has suggested that hermaphroditism,
parthenogenesis and related phenomena are Gene Dispersal Model
advantageous in unstable environments that
are frequently depopulated. Clearly, if a A third hypothesis is the gene dispersal model.
localized population were reduced to as few as It is based upon the idea that limitations upon
two members, it would have twice the proba- dispersal may affect population structure, or
bility of survival if their members were simul- what Mayr (1954) has called the "genetical
taneous hermaphrodites. The low density environment." Under certain conditions, the
model does not always suffice to account for availability of optimal mates is restricted by
many instances of hermaphroditism. Ordinar- lack of motility, and hermaphroditism may
ily it is not workable for sequential hermaphro- help to overcome the difficulties. At least two
ditism, such as in protandry (where the animal such effects seem plausible, so that we may
begins its period of reproduction as a male, recognize two versions of this hypothesis: the
then is transformed into a female) or proterog- inbreeding version and the sampling-error
yny (where it changes from female to male). version.

JUNE 1969] EVOLUTION OF HERMAPHRODITISM 191
The inbreeding version is based upon the of animals (Geiser, 1923). Evidence will be
fact, well-known to botanists that protandry given here suggesting not only that such aber-
and proterogyny help to prevent inbreeding ration occurs where gene-dispersal is restricted,
by self-fertilization. We need only extend this but also that hermaphroditism evolves under
idea to see that sequential hermaphroditism the same conditions. Note that group selection
may reduce the probability of inbreeding need not be invoked, for if an individual mates
among siblings. If all members of a brood as often as possible, the probability of having
were to grow at the same rate, and all to pass, at least some viable offspring should increase,
simultaneously, first through a male stage and irrespective of any accidental benefits to the
then through a female stage, they would not group.
be able to cross with one another. A similar Since the gene dispersal model may not
phenomenon is merogony, in which an indi- seem novel, it is important to see just what
vidual has offspring all of the same sex. An- is, in fact, new; in order to avoid misinter-
other way to decrease the probability of sibling pretations, certain conceptual difficulties need
crosses is to have a period of vegetative or to be analyzed and made explicit. Let us con-
parthenogenetic reproduction intervening after sider how the activities of organisms may be
birth, giving slow-moving relatives time to dis- treated at various levels of integration: cellular,
perse. (For a discussion of possible selective organismal, and a variety of population levels.
advantages of a tendency to migrate, see It has become increasingly evident how difficult
Lidicker, 1962.) Fisher (1965: 130-136) has it is to deal with phenomena in which the
suggested that parent-offspring crosses are more effect of action at one level may have a complex
frequent in sequential hermaphrodites, but impact upon another. It is especially important
some other influence could easily offset this to avoid slipping from one level to another.
effect. For example, in the low density model, dis-
The sampling-error version is based upon the persal is important; and, conversely, density
fact that genetical environment is also influ- may also have some effect where dispersal is
enced by genetic drift and analogous phenomena the problem. In the low density model, how-
in small isolated populations (Wright, 1938). In ever, the functional influence is the dispersal
small populations there frequently will be a of individuals relative to each other, while in
numerical excess of one sex, thereby decreasing the gene dispersal model, we are concerned
the variety of possible crosses and lowering the with situations in which the flow of genes in
effective population size. Murray (1964) argues and between populations is limited.
that a 1:1 effective sex-ratio, the necessary The controversy over group selection, which
consequence of simultaneous hermaphroditism, has much bearing upon the subject of her-
would maximize the effective population size. maphroditism, likewise involves conceptual
He also points out that in hermaphroditic ter- difficulties related to hierarchical level. Natural
restrial snails, multiple matings and sperm selection, in the strict sense, involves only the
storage are capable of producing a similar effect. differential survival of individuals within the
Both inbreeding and sampling error have same genetical population (Darwin, 1859;
the same consequence: reducing genetic varia- Williams, 1966). The differential extinction of
bility. They occur under similar conditions, whole groups is not the same type of phe-
however, and their effects are not easily dis- nomenon, afthough the two are often confused.
tinguishable in practice. Hermaphroditism Non-Darwinian (group) selection may have
would compensate for both of these effects of considerable evolutionary effect. Pre-adapta-
limited gene dispersal, and perhaps for others tion, in the sense of antecedent fitness (Ghiselin,
as well. Although our theoretical understand- 1966a) may further the success of whole line-
ing of the effects of population size and in- ages. Stebbins (1950: 70), for example, has
breeding upon the sex-ratio is fairly rudimen- drawn attention to the fact that in plants a
tary (Andersen, 1961; Kimura and Crow, 1963), combination of long life and outcrossing results
it has long been known that the sex-ratio in long-term success, owing to greater evolu-
deviates considerably from 1:1 in various groups tionary flexibility. On the other hand, short-

lived selfers do well where immediate fitness ber of phenomena such as mimetic polymor-
is crucial; in the long run they tend to vary less, phism could be treated in the same way. It
however, and are less successful. would seem, therefore, that the gene dispersal
In explaining the evolution of sexuality and model is a kind of theory which has only begun
a number of its features, including hermaphro- to be investigated.
ditism and parthenogenesis, differential extinc-
tion and group selection hypotheses have fre- TESTING THE HYPOTHESES
quently been invoked. Early Mendelians (Mul-
ler, 1932) and some others (Fisher, 1930; General Considerations
Darlington, 1958: 231-234) could see no value
to the individual in crossing, and therefore held Once a series of hypotheses has been enunci-
that sex must subserve long-term evolutionary ated, the methodology of testing them must be
success. But this kind of explanation fails to ac- considered. Obviously, the problem is too
count for the increase of genes for sexuality large and novel to be settled experimentally
within the population. Many have sought to at this stage; therefore, I have used the litera-
treat the origin of supposedly altruistic prop- ture as the basis for a comparative study. Since
erties as a consequence of kinship selection: the literature on hermaphroditism is enormous,
there is an adaptive advantage to furthering even if one omits its teratological and physio-
the survival of genotypes similar to one's own. logical aspects, the discussion is restricted to
This is only one way to analyze the problem, evidence which seems to bear directly on the
and not necessarily the most effective one. problem of how and why hermaphroditism
Another way is to view supra-individual, inte- develops. The type of comparative approach
grated systems as fundamental units of selec- employed here, although not currently fash-
tion. Thus, Darwin (1859) explained the origin ionable, may be defended on the basis of its
of neuter castes in social insects by treating the impressive results (Harvey, 1628; Darwin, 1859).
family as the unit of selection. Upon a more The procedure, involving as it does, hypoth-
general level, we might say that a parent may esis, prediction, and refutation, is as valid
distribute genes among its offspring in such a as a laboratory experiment. But it is more
manner that the offspring as a group are more difficult. A primary stumbling block is the
likely to survive. Sexual reproduction may be existence here of three major hypotheses which
selected in just such a manner. Crossing has do not invariably contradict each other. It
often been thought of as promoting direct and would be very easy to indulge in ad hoc
immediate advantage to the individual, through rationalization, and to construct a set of explan-
heterosis or what Darwin (1876: 254) called ations that would cover any logically possible
"differentiation in the sexual elements." This observations. But the basic point is frequently
view has rather simplistically been questioned missed, as, for example, by those who have
(Muller, 1932: 119) on the grounds that inbred charged that this is a defect of the synthetic
theory of evolution. For Darwin himself states:
lines are purged, through selection, of deleteri-
"If it could be proved that any part of the
ous recessives. But in addition, we should not
structure of any one species had been formed
overlook the possibility that variability, the
for the exclusive good of another species, it
result of crossing, may have quite a number of
would annihilate my theory, for such could
subtler effects at supra-individual levels, which
not have been produced through natural selec-
can also be selected. Thus, if the young of a tion" (1859:201). The properly designed com-
mammal were all genetically alike, the proba- parative study (e.g., Darwin, 1871) focuses upon
bility might be increased that all of them would those particular observations which do in fact
die in a plague (leaving the parents potentially provide critical tests of one or more out of a
able to expend surplus energy on raising young, set of contrary hypotheses.
but with no young to raise). Were only some In evaluating the various hypotheses, I shall
of the offspring to die, more energy would be review those conditions in which there has
available for the care of the survivors, and the been a shift in habitat or way of life corre-
result would be a selective advantage. A num- lated with the evolution of the hermaphroditic

state. These will include situations in which niques are available. One may infer that her-
some of the models apply and others do not, maphroditism existed before any hypothesized
although ambiguous data are included for com- selection pressure was active by demonstrating
pleteness of discussion. In order to provide its presence in related forms not subject to
independent evidence that the particular selec- that selection pressure. To establish post-
tive influences invoked are in fact responsible adaptive change, one need only show that
for the observed changes, a version of Bock's multiple pathways have been adopted, or that
principle of multiple pathways of adaptation a taxon subject to the hypothesized selection
(Bock, 1959) is sometimes invoked. Bock's pressure includes forms which have as yet not
principle states that when a group of orga- adapted to it. I reject as covertly metaphysical
nisms adapt to a particular selective influence, the notion that adaptation is necessarily in-
they may (but need not) do so by adopting stantaneous, and that, therefore, historical
divergent mechanisms which deal with the same antecedents are irrelevant to ecology (Birch
functional problem. Where such divergence is and Ehrlich, 1967); one need only answer that
demonstrable, but not otherwise, certain his- the probability of a variation may sometimes
torical inferences are valid. The implication be less than one (Darwin, 1859, 1871).
to be derived here is that if there is a shift to We may expect a restriction in the rate of
hermaphroditism, one of the selective influences movement of genetic material to have occurred
inherent in the models may be adapted to in repeatedly in the evolution of marine orga-
a variety of ways, some of which are not adap- nisms. Many benthic forms have larvae or pe-
tive to the other selective influences. Being lagic eggs, allowing the young to be carried vast
in a position to know, for a variety of par- distances by currents. Barriers to gene flow
ticular situations, what kind of selection pres- are quite limited, as they are in strictly pelagic
sures can or cannot be invoked, we may con- organisms. Such passive dispersal has been lost
struct a comprehensive system which tests the in the many marine invertebrates which no
various hypotheses. Thus, where the low den- longer have larvae. In both these and in ter-
sity model should be expected to apply, as in restrial and fresh-water forms, there has been
parasites and sessile organisms, there should be an obvious change in population structure.
simultaneous hermaphroditism and phenomena The implications of this fact are numerous,
of the dwarf-male type, although other factors but they have not yet received their due con-
might interfere to prevent the evolution of sideration. It has been noted, for instance,
either or both. Simultaneous hermaphroditism that marine gastropods are very stable in
would be consistent with the gene dispersal chromosome number, while fresh-water and
model, but not the size advantage model; the terrestrial forms vary greatly (Burch, 1965;
converse relation would hold for the dwarf Patterson, 1967). Elimination of a larval stage
males, and their joint implication could be has evidently increased the frequency of foun-
used to exclude both. Again, under ecological der effects and other types of sampling error.
conditions to which the gene dispersal model It is also interesting to consider what goes on
would apply, one should look for such phe- in the deep sea, where, although species di-
nomena as sequential hermaphroditism and versity is high, population density is low
meregony, which will not, respectively, adapt (Hessler and Sanders, 1967); here, simultaneous
the individual to low density and size influences. hermaphroditism ought to be quite pronounced.
The effects of size advantage will appear under
particular kinds of ecological conditions; se- Systematic Review
quentiality will be involved and will tend to Porifera are mostly hermaphroditic, with a
coexist with marked sexual dimorphism. The few sequentially so, or gonochoric (separate-
hypothesis that a given case of proterogyny is sexed) (Hyman, 1940). The lack of comprehen-
due to sexual selection may be evaluated by sive data restricts critical study. Although a larva
means of Darwin's (1871) canons of evidence. is present, and sessility implies the low density
In determining whether hermaphroditism was model, the few instances of sequential her-
pre-adaptive or post-adaptive, a variety of tech- maphroditism leave some room for doubt. As

in plants, asexual reproduction complicates the model is preferable. The increased asexual
problem. reproduction among terrestrial forms (Hyman,
Cnidaria are usually gonochorists, but scat- 1951a) is perhaps due to dispersal effects; selfing
tered exceptions have been reported (Hyman, among turbellarians is rare (Anderson, 1952).
1940). The hydrozoa are mostly gonochorists, The Trematoda are simultaneous hermaphro-
and the occasional hermaphrodites (Foyn, dites, except for the families Didymozoonidae
1927: 516) could be explained in various ways. and Schistosomatidae, in which the sexes have
In alcyonarians and anthozoans, the few her- separated secondarily, and the males and fe-
maphrodites tend to be sequential (Hyman, males live in close association. As one would
1940). In anemones, there is some correlation expect for parasites, only the low density model
between hermaphroditism and viviparity (Gra- applies. The Cestoda, or tapeworms, are strik-
vier, 1916), although only a minority of vivip- ingly similar, all being simultaneous hermaphro-
arous forms, and others in which the larva dites, except for Dioecocestus, which is sec-
is rather suppressed, are known to be her- ondarily gonochoric.
maphroditic (Carlgren, 1901). A study by The Rhyncocoela, or nemerteans, are gen-
Stephenson (1929) on 8 species of sea anemones, erally marine, free-living gonochorists, although
revealed that the 6 gonochoric species have hermaphroditism is widespread throughout the
both asexual reproduction and free-swimming group (Gontcharoff, 1961). As a rule, the
larvae. The two hermaphroditic species are hermaphrodites are not marine (Hyman, 1951a:
brooders with no asexual reproduction. One 492), or else they are not free-living, as with
of these is larviparous and hermaphroditic a commensal species (Coe, 1938) and a parasitic
only near England; elsewhere it is oviparous genus (Keferstein, 1868; Marion, 1873). A fairly
and gonochoric (Thorson, 1946). This sort of high frequency of aberrant sex ratios and se-
geographical pattern, very common where larval quential hermaphroditism lends weight to the
type varies, gives us reason to infer that selec- gene dispersal model, especially among terres-
tion is operating. That hermaphroditism tends trial (Coe, 1939) and freshwater (Moore, 1895)
to be sequential and that forms with a pelagic forms.
dispersal mechanism are gonochorists argue The Acanthocephala, although parasitic, are
against a low density interpretation in this gonochorists (Hyman, 1951b).
context. Both types have a means (asexual The Rotifera are exclusively gonochoric
reproduction or brooding) of insuring a high (Hyman, 1951b; de Beauchamp, 1965). The
local population level. The forms with pelagic well-known cyclic parthenogenesis of some roti-
larvae receive genes from other populations and fers has often been explained by versions of the
hence have no sampling or inbreeding problems. low density model. The inbreeding model or
Either version of the gene dispersal model, the sampling-error model may well prove ap-
perhaps both, would work for the hermaphro- plicable to this parthenogenesis, however, since
dites. a period without crossing would allow a longer
The Ctenophora are all hermaphrodites, period for close relatives to move to a position
either simultaneous or else protandrous and where they would be likely to outcross. Birky
able to store sperm, which would have much the (1967) has shown that Asplanchna is not an
same functional effect. They are pelagic, or extreme inbreeder, and that deleterious reces-
benthic with little motility as adults, but in- sives are expressed in inbreeding experiments.
variably have some motile period in their life The Gastrotricha have many points in com-
cycle. Thus the sexual biology and way of life mon with rotifers. The Macrodasyoidea are
are strictly consistent with the low density largely marine and hermaphroditic, while the
model. Chaetonotoidea are fresh-water and partheno-
The Platyhelminthes will be treated class genetic (except for two marine genera). The
by class. The Turbellaria are, if we except one data (cf. Hyman, 1951b: 167-169) are consistent
family that tends to be gonochoric, simultaneous with a shift from conditions where the low
hermaphrodites. The marine forms usually density model should apply (the sea) to those
have a good larval stage; hence the low density where rapid multiplication has become increas-

ingly significant and gene dispersal effects are disagree as to whether certain forms are gono-
more common (fresh water). For both rotifers chorists or sequential hermaphrodites (Marcus,
are gastrotrichs it may prove very revealing to 1949; Rattenby, 1953; Silen, 1954; Dawydoff,
compare the inhabitants of seasonally stable 1959). The low density model would be a rea-
tropical lakes with those in which conditions sonably conservative interpretation, as the larval
are more variable. stage is not wholly suppressed.
The phyla Kinorhyncha and Priapulida are For the Ectoprocta, sessility correlating with
marine, free-living, and gonochoric. widespread hermaphroditism (Hyman, 1959)
Marine and parasitic Nematoda generally supports the low density model. The occasional
have a 1:1 sex ratio, but in fresh-water and ter- proterogyny and protandry may block crosses
restrial forms there tends to be an excess of within the colony. Sil6n (1966) has shown that
females (de Conick, 1965). Dispersal problems outcrossing definitely occurs, contrary to some
as a cause for deviation in sex ratio seem the older views.
best explanation here, for the dispersal of free- All Chaetognatha are either simultaneous
living, marine forms by currents, and of para- hermaphrodites, or the functional equivalent,
sitic forms by their hosts, makes the data for since they store sperm (Hyman, 1959). As
both types fit a consistent pattern. Terrestrial chaetognaths are almost all pelagic, and display
nematodes are often self-fertilizing or partheno- evidence of selfing in certain instances, only
genetic, and this may be combined with her- the low density model need be applied here.
maphroditism (Maupas, 1900; Honda, 1925; The exclusively marine phylum Sipunculida
Nigon, 1949a, 1949b). are as a rule gonochorists with a larva. The sole
The Nematomorpha are gonochoric parasites exception, Golfingia minuta, a minute brooder,
(Dorier, 1965). That hermaphroditism has not is hermaphroditic when young, but female
evolved in this group could be due to its not later on, except that an American form may be
being physiologically advantageous, but perhaps proterogynous (Akesson, 1958). The gene dis-
it relates to the dispersal powers of the hosts persal model would fit both populations.
or of the adults, which are free-living. The Echiuroidea are marine, gonochoric, and
The Endoprocta are sessile, reproduce asexu- pelagic in development. The celebrated dwarf
ally to varying degrees, and are usually gono- males of the Bonellidae, which Zenkevitch
choric (Hyman, 1951b). In the fresh-water genus (1966) relates to deep-water conditions, are
Urnatella one species is gonochoric (Emscher- clearly in line with the low density model.
mann, 1965), the other a simultaneous her- The phylum Annelida is subdivided for con-
maphrodite (Seshaiya, 1949). The protandry in venience. The Archiannelida are small, and
Loxosomella vivipara discovered by Nielsen often brooders. In this group as elsewhere, the
(1966) is inconclusive, as there would appear correlation between small size and brooding
to be a fairly good dispersal. evidently has to do with the fact that a limited
The only known hermaphroditic Brachiopoda number of eggs makes it improbable that any
are the genera Pumulus and Agyrotheca (de member of a clutch will survive through the
Beauchamp, 1960). The three species of the larval period (Ghiselin, 1963). Simultaneous
latter genus studied by Senn (1934) were brood- hermaphroditism in forms with larvae (Hempel-
ers, but there would appear to be a very brief mann, 1906), aberrant sex ratios and partheno-
swimming stage (Oehlert and Deniker, 1883). genesis (de Beauchamp, 1910) and dwarf male
In Pumulus, the large ova are highly suggestive phenomena (Pierantoni, 1907, 1908) show that
of abbreviated development, hence limited dis- the low density model must be invoked in addi-
persal (Atkins, 1959). These facts would lead tion to any dispersal effects.
us to infer that only a partial restriction of gene The hermaphroditism of the Polychaeta is
flow suffices to give advantage to hermaphro- widely distributed systematically, and therefore
ditism. may be considered a polyphyletic adaptation
The Phoronida are sessile, usually hermaphro- to special conditions. Mesnil and Caullery
ditic animals (Hyman, 1959). Although many (1898a,b) drew attention to a correlation
are simultaneous hermaphrodites, authorities between protandry, asexual reproduction and

direct development (cf. Dehorne, 1919; Vannini, In the Arenicolidae, Branchiomaldone vin-
1950; Fauvel, 1959). Here, protandry is clearly centi broods its young and is a simultaneous
referable to the inbreeding model, or to the hermaphrodite which does not reproduce
effects of sex-ratio (sampling-error model). asexually (Ashworth, 1913).
Vegetative reproduction will help to offset local In the Dorviellidae, Ophyrotrocha puerilis,
low densities, or to prevent the entire local with the pelagic stage repressed in at least some
population from being wiped out. Conditions parts of its range (Thorson, 1946), evidently
here are thus quite different from those in the varies geographically in the proportion of pure
Anthozoa and in trees, where asexual repro- male, pure female, and protandrously her-
duction and the gonochoric state correlate with maphroditic forms and stages (Korschelt, 1894;
fairly effective dispersal mechanisms. Huth, 1933; Muller, 1962; Bacci and Bortesi,
Sagitella is a simultaneous hermaphrodite 1961). Bacci (1965a,b) has altered the sex ratio
with direct development; as it is pelagic, the low by artificial selection. Purely hermaphroditic
density model fits best (Uljanin, 1878). Hesione are 0. hartmani, 0. gracilis (cf. Huth, 1933) and
sicula is protandrous (Bergmann, 1902). 0. labronica (Parenti, 1960). We have here
In the Syllidae, Prionosyllis neapolitana is an the general sort of pattern observed in Actinaria
hermaphrodite brooder, unlike its close rela- and elsewhere. If the degree of hermaphro-
tives, which, although brooders, are gonochorists ditism should be found to correlate with local
(Goodrich, 1930). Grubea has direct develop- differences in dispersal ability, the foregoing
ment, with G. proton drica protandric (du facts would take on added significance.
Plessis, 1908), G. clavata having some individuals Among sabellids, Sabella micropthalmia has
purely male, others hermaphroditic with an female and hermaphrodite individuals (Gregory,
initial female phase (Hauenschild, 1953, 1959), 1905). Dasychone cingulata's hermaphroditism
and G. pusilloides a simultaneous hermaphro- has been attributed to "sedentary habits" and
dite (Haswell, 1918). Syllis corruscans combines "fluctuating environment" by Aiyar and Sub-
asexual reproduction with proterogyny (Has- ramaniam (1937: 242).
well, 1885), while S. vivipara is parthenogenetic For the Serpulidae, a great deal of material
(Goodrich, 1900; Potts, 1911). In this family, is available on the small, tubiculous Spirorbis.
the gene dispersal model alone seems both Thorson (1946) notes that S. spirillum is gono-
necessary and sufficient. choric, and does not brood its young, while
In the Nereidae, Lycastis indica is a protan- S. borealis is an hermaphrodite brooder. Ac-
drous to simultaneous hermaphrodite (Aiyar, cording to zur Loye (1908) the latter species is
1935), while L. quadraticeps is said to be a protandrous and has a very short larval life.
simultaneous hermaphrodite with direct devel- The hermaphroditism is simultaneous in this
opment (Johnson, 1908); the penetration of both species according to Bergan (1953) and also in
species into fresh water would tend to restrict S. pagenstecheri (Gee and Williams, 1965) and
gene flow. According to R. I. Smith (1950, in S. moerchi (Potswald, 1967)-both of which
1958), Nereis limnicola is viviparous and self- have some form of brood protection. The low
fertilizing. Nereis diversicolor, a euryhaline density model is favored by the fact of sessility,
form in which the pelagic phase has been sup- yet the gene dispersal model is not excluded,
pressed, displays a highly variable sex ratio as the larval period is exceedingly brief
(Dales, 1950; Bogucki, 1954). Conditions in (Pagenstecher, 1863; Schivley, 1897; Thorson,
Platynereis, a form with direct development, 1946; Bergan, 1953). Only low density seems
are most revealing: P. dumerilii has a swim- consistent with the rather meager evidence for
ming, adult dispersal stage, and is gonochoric facultative self-fertilization (Gee and Williams,
(Abeloos, 1950; Durchon, 1955), while the her- 1965; Potswald, 1967). In Filograna implexa
maphroditic P. massilensis has no such dispersal and Salmacina dysteri, asexual reproduction,
mechanism. A case might be made for either direct development and simultaneous her-
the low density model or the gene dispersal maphroditism coexist (Huxley, 1855; Saint-
model, but we may at least observe a consistent Joseph, 1894; Thorson, 1946); Malaquin (1911)
pattern here. reported variations in the percentage of her-

maphrodites with both space and time. The have repeatedly evolved from the gonochoric
aberrant sex ratio of Pomatoceros triquiter, a to the hermaphroditic state. The occurrence
form with short pelagic life (Thorson, 1946) of hermaphroditism in highly specialized feed-
has been attributed to protandry (Foyn and ers, including parasites, supports the low den-
Gjoen, 1950); a size advantage model might sity model (Ghiselin, 1966b). Protandry, which
find application here. sometimes varies geographically, would seem to
A maldanid, Caesicirrus neglectus, has various be most frequent among various unrelated
percentages of hermaphrodite individuals, but groups of intertidal limpets; it is best explained
the reason for this phenomenon in unknown by the size advantage model (Bacci, 1947a, b, c,
(Pilgrim, 1964). 1951a; Coe, 1944, 1948). The otherwise exclu-
The Oligochaeta are all hermaphroditic, with- sively gonochoric neogastropods have one pro-
out a dispersal stage, and frequently have tandrous hermaphrodite, Lora turricula (cf.
asexual reproduction and parthenogenesis E. H. Smith, 1967). Smith suggests that isolated
(Avel, 1959). The low density model is plausi- populations might benefit by having both males
ble, although dispersal effects may also be and females present. Protandry, however, would
important. counteract this effect. As this species has no free
The Hirudinea, being parasitic and simul- larval stage whatsoever (Fretter and Graham,
taneous hermaphrodites, clearly fit the low 1962), the dispersal model may be considered
density model (Harlant and Grasse, 1959). the best explanation. Hermaphroditism, vir-
The Myzostomida are all marine. They para- tually always simultaneous, is characteristic of
sitize echinoderms, especially crinoids, and have the Euthyneura, a group including most species
a well-developed larval stage. Some are func- and orders of gastropods (Ghiselin, 1966b). The
tional simultaneous hermaphrodites, but there marine forms either store sperm or are other-
would seem to exist an evolutionary trend wise functionally simultaneous hermaphrodites.
toward protandry, with facultatively dwarf- Proterogyny (Rosenwald, 1926; Hoffman, 1927)
male stages coexisting with females (Beard, is rare, and is known only among land snails
(Pulmonata). Since the terrestrial pulmonates
1894; Wheeler, 1894, 1897; Prenant, 1959). The
low density adaptations of cirripedes and echiu- have descended, polyphyletically, from marine
roids are strikingly parallel. forms with good larvae, it is hard to invoke the
gene dispersal model to account for the origin
For the Mollusca, the useful reviews of
of their hermaphroditism. But their proterogyny
Pelseneer (1895) Fretter and Graham (1964)
is crucial evidence for its now subserving this
and others allow a relatively summary treat-
Kind of function, for unlike that of protandrous
ment, one which will be subdivided into classes.
forms that store sperm, it would not adapt in
The Polyplacophora, or chitons, have one
relation to low density.
hermaphrodite species, Cyanoplax dentiens,
Hermaphroditism in the Bivalvia wa? long
which is also a brooder, living isolated in high
ago reduced to a series of empirical rules by
tide pools (Heath, 1908). Thirteen of the
Pelseneer (1912), who could not explain them
approximately 500 described species of chitons
are known to have some form of brood protec- (cf. Coe, 1943; Fretter and Graham, 1964). He
tion (A. G. Smith, 1966). The dispersal model noted that hermaphrodites may largely be
obviously applies. divided into: (a) commensals; (b) deep-sea
Among the Aplacophora, or solenogasteres, forms, and (c) forms that incubate. The first
the free-living forms are gonochorists, while and second classes are best covered by the low
those commensal with, or parasitic upon, hy- density model, although the occurrence of
droids are hermaphrodites. Although these brooding in many forms means that we cannot
latter have been considered protandrous, they rule out other possibilities. Those that incubate
store sperm. As a well-developed larval stage are sometimes protandrous (Hansen, 1953; Sell-
is present, only the low density model need be mer, 1967). However, the occurrence of her-
invoked. maphroditism, occasionally successive, in various
The Monoplachophora, Scaphopoda and forms with a free-swimming larva, demonstrates
Cephalopoda are gonochorists. The Gastropoda that the relationship is not altogether simple

(cf. Pelseneer, 1912; Dalmon, 1938; Lubet, 1953, model. (e) Beach-hoppers (which are amphi-
Lucas and Franc, 1962). Particularly suggestive pods) have reduced the dispersal stage and dis-
evidence is available for freshwater mussels. play an apparent tendency in the same direction
The sexes are ordinarily separate, but in quite as terrestrial and fresh-water crustations (cf.
a number of species hermaphrodite individuals below). Their populations sometimes include
are rather common (Le Fevre and Curtis, 1912; hermaphrodites, but these are thought not to
Bloomer, 1939; Van der Schalie, 1966). The be functional (Boulenger, 1908; Sexton and
young are readily distributed, at least within Huxley, 1921; David, 1936; Steele, 1967). (f)
a single body of water, by the larval stage Fresh-water and terrestrial isopods have fea-
(glochidium), which is parasitic on fish. tures which are hard to explain except on the
Weisensee (1916) studied populations from basis of the gene dispersal model, particularly
rivers, and from ponds separated from the river the inbreeding version. The sex ratio often
for up to three hundred years. In the Rhine he deviates from 1:1 (Vandel, 1925). Hermaphro-
found a sex-ratio of 1:1. With increasing time ditism, usually protandric, is known (Jackson,
of isolation, the females began to preponderate 1928; Arcangelli, 1932). Merogony is frequent
over males, then hermaphrodites appeared and (de Lattin, 1952); Vandel (1941) considered it
gradually replaced the gonochorists. Here we detrimental to the species, but under conditions
have a good example of the effects of restricted of inbreeding, it may nonetheless be advan-
dispersal, perhaps working through the dis- tageous to the individual. (g) Among insects,
turbance of sex-ratio. It has not been merely a the rarity of hermaphroditism correlates with
pre-adaptive feature. dispersal by flying; the analogy with marine
In the Arthropoda, much as in bivalves, forms having a larval stage should be obvious.
various taxonomic and ecological distributions Parthenogenesis in the non-motile stage may
of hermaphroditism may be seen to correlate equally well be compared with asexual repro-
with particular selective influences. (a) Deep- duction in the benthic stages of those coelen-
sea crustaceans, again, show a higher instance terates with a medusa stage. Functional her-
of hermaphroditism than do shallow water maphroditism has evolved in a wingless fly,
forms (Wolff, 1956, 1962). Records of normal Termitoxenia, which lives as a commensal in
hermaphroditism among free-living forms are termite nests (Wasmann, 1900, 1902; Assmuth,
rare (Spitschakoff, 1912; Dohrn, 1950; Lang, 1923; Megelsberg, 1935).
1958; Heegard, 1967). (b) Parasitic crustaceans The Echinodermata have two wholly gono-
display two patterns characteristic of low-density choric classes: Crinoidea and Echinoidea
conditions: (1) hermaphroditism and partheno- (Hyman, 1955; Harvey, 1956). In the Ophi-
genesis (Bullar, 1877; Mayer, 1878; Montalenti, uroidea Mortensen (1936) pointed out, but
1941); and (2) phenomena of the dwarf-male could not explain, a correlation between brood-
type (Delage, 1884; Caullery, 1908; Reverberi ing and hermaphroditism. At the time it was
and Pitotti, 1942; Reinhard, 1942, 1949). (c) Bar- known that among 54 viviparous species, 9
nacles, as has been mentioned, are similar; were gonochorists, 2 or 3 parthenogenetic, and
they are thought to be facultatively capable of 36 hermaphrodites (including 1 facultative and
self-fertilization or parthenogenesis (Barnes and 9 protandric). At least up until Hyman's (1955)
Crisp, 1956). (d) Some notostracans live in fresh- review, all hermaphroditic ophiuroids were
water pools of a very temporary nature. They thought to have had some form of brood pro-
have been said to display atypical sex ratios, tection, and no exceptions were known. The
parthenogenesis, and various proportions of fairly high instances of protandry favors the
hermaphroditism (Benham, 1896; Bernard, gene dispersal model. A few species (4 accord-
1896). Triops cancriformis populations show a ing to Hyman, 1955) have dwarf males, and
northward, clinal decrease in the proportion of therefore low density effects cannot be alto-
males, while those from rice fields are all gono- gether excluded. In the Asteroidea, forms with
chorists (Longhurst, 1955a,b). Fewer her- a reduced larval stage tend to be hermaphro-
maphrodites among more stable and permanent ditic, but the general pattern is more what one
populations are suggestive of the sampling-error would expect from the size advantage model

rather than the gene dispersal model. Asterias ered by a few general rules having to do with
forbesi is protandric (Aldrich and Aldrich, their way of life:
1955), but has a larva. Hermaphroditism has (a) In deep-sea fishes the low density model
been recorded as occurring in 1% of the indi- applies in a manner strikingly reminiscent of
viduals of Marthasterias glacialis populations crustaceans and bivalves. Fish of the order
(Delavault and Cognetti, 1961), and up to 4% Iniomi, with good motility, are simultaneous
in Echinaster sepositus (cf. Delavault, 1961). In hermaphrodites (Mead, 1960; Nielsen, 1966).
the genus Asterina the larva is suppressed (b) The size advantage model would seem the
(Mortensen, 1933). Individuals of A. batheri only available explanation for many instances
differ in the extent of hermaphroditism of sequential hermaphroditism. This is espe-
(Oshima, 1929). Cuenot (1898) observed that cially true of shallow water marine fishes, some
the sexuality of Asterina gibbosa varies geo- of which are simultaneous hermaphrodites, but
graphically: at Roscoff, all were protandric; at an unusually large proportion are protandrous
Banyuls, some simultaneous hermaphrodites or proterogynous (Reinboth, 1962; C. L. Smith,
were found; the Naples population tended 1959, 1965). In this context, it is particularly
toward gonochorism, with some purely male interesting that Breder and Rosen (1966) have
and female individuals along with the her- noted a tendency toward larger females where
maphrodites (cf. Bacci, 1951b; Hauenschild, many eggs are laid, and that the sex which
1954; Delavault, 1960; Cognetti and Delavault, broods the eggs is usually the larger one. The
1962; Brusle, 1968). A. pancerii is proterogy- existence of sexual selection is attested by the
nous, and perhaps facultatively self-fertilizing, marked difference in coloration of the males in
or else parthenogenetic (Cognetti, 1954, 1956). proterogynous forms (Lonnberg and Gustafson,
The brood care and viviparity of certain 1936; R6gnier, 1938; Zei, 1949; Lavenda, 1949;
Holothuroidea have been the subject of a num- Bacci and Razzauti, 1958; Reinboth, 1962).
C. L. Smith (1967) has elaborated a series of
ber of reviews (Ludwig, 1904; Vaney, 1925;
models, which amount to versions of the size-
Hyman, 1959), but these do not attempt to
advantage model, although size, as such, is not
assess the possible correlation with hermaphro-
treated as the basic consideration. He argues
ditism. Protection of the young has evolved
that in polygamous forms, various kinds of
several times, as may be demonstrated by its hermaphroditism might compensate for the
involving external brood pouches of diverse effects of inequalities in reproductive potential.
morphology in the Cucumariidae, and viviparity He suggests that if sequential hermaphroditism
in the Synaptidae, with closely related forms results in a longer life-span, it might be favored
retaining the original free-swimming larvae under certain conditions. Although of the
(Vaney, 1925). Of the 9 species of Cucumariinae highest theoretical interest, these models show
listed as brooders by Vaney (1925), at least 4 little obvious applicability to conditions known
are hermaphrodites (Ackermann, 1902; Ludwig, to exist in nature. The correlation of polygamy
1904; Vaney, 1925); of 4 viviparous Synaptidae, with sequential hermaphroditism is as consistent
there are a gonochorist and three hermaphro- with the sexual selection hypothesis as with the
dites-to which we may add three additional size-advantage hypothesis; the former hypothesis
gonochorists (Ludwig, 1904; Becher, 1906, 1907; has the further advantage of explaining the
John, 1939). Mesothuria intestinalis, not re- polygamy itself. In addition, the idea that "In
ported to brood, is also an hermaphrodite. The a real population, the presence of excess males
same phenomena thus seem evident in both or excess females could be advantageous"
holothurians and ophiuroids. (Smith, 1967:79) needs to be elaborated to
In the phylum Chordata, the sessile Tunicates show how the individual is benefitted. We also
are virtually all simultaneous hermaphrodites, need predictions from theory and experiential
as predicted by the low density and gene dis- tests. Smith's hypotheses, intended to account
persal models; the proterogyny of salps may for conditions in fish, would seem to have less
perhaps be referred to their budding (Castle, explanatory value for invertebrates, in which
1896; Brien, 1948). Fish (Atz, 1964) are cov- the mating systems differ considerably. They

also do not account for the general ecological vironment in the more usual sense, but also
rules applicable to all organisms. Nonetheless, upon the structure of the population wherein
they may prove useful when the data are re- reproductive transactions occur. Differences in
examined in greater detail. Another point that population density, in gene flow, and in other
needs to be cleared up is that some of the circumstances, provide a wide range of condi-
protandry is due to an indifferent juvenile tions under which the reproductive apparatus
stage (Kinoshita, 1939) or to facultative selfing may evolve. Although there is no single ex-
(Clark, 1959). planation for the many instances of hermaphro-
(c) In freshwater fishes, the gene dispersal ditism, virtually all may be covered by a few
model, in both sampling-error and inbreeding rules, which in turn relate to a group of theo-
form, explains much. The protandry of Cobitis retical models:
taenea L. (Lodi, 1967) fits in well with the gene The low density model invokes the advantage
dispersal model. Disturbances of the sex-ratio of being able to mate with any other member
are common in fresh-water fish (Huxley, 1920; of the species where the probability of en-
Essenberg, 1923; Bullough, 1940; Lieder, 1959; countering a suitable mate is low; it predicts
Miller, 1962), as is typical of high inbreeding the frequent occurrence of hermaphroditism
conditions. Yet selfing, parthenogenesis etc. and certain other sexual arrangements among
show that low-density effects may have consider- sessile organisms, deep-sea animals and para-
able influence (Hubbs and Hubbs, 1932; Lieder, sites.
1955; Spurway, 1957; Haskins, Haskins, and The size advantage model explains sequential
Hewitt, 1960; Harrington, 1961, 1967; Schultz, hermaphroditism as occurring where an indi-
1961; Kallman, 1962a, 1962b; Kallman and vidual reproduces most efficiently as a member
Harrington, 1964). The insufficiency of the low- of one sex when small or young, but as a
density model, however, is obvious from com- member of the other sex when it gets older or
parative studies on marine and estuarine popu- larger; it predicts proterogyny where there is
lations of smelt (Osmerus) (Hoffmeister, 1939; sexual selection for larger males, and protandry
Lillelund, 1965). In the open sea, hermaphro- where the young stages must hunt for a suitable
dites are unknown, and the sex-ratio is 1:1. In environment.
the Elbe estuary, the females preponderate, The gene dispersal model is based upon the
evidently because of a higher male mortality idea that the individual may be adapted to the
(Lillelund, 1965), and hermaphrodites are genetical environment, or to the population
common. The analogy of these studies with structure as affected by the prevailing condi-
those on fresh-water mussels is indeed re- tions of gene flow. In the inbreeding version
markable. Perhaps C. L. Smith's models will it is hypothesized that where motility is re-
apply here, but if so, they are far from stricted, sibling crosses become more frequent,
sufficient. Liem (1968) invokes a group-selec- and that various mating systems, especially
tionist version of the low density model for the sequential hermaphroditism, will reduce their
freshwater Synbranchiformes; it is hard to see effects. In the sampling-error version, her-
how to make this mechanism work in these maphroditism is conceived of as an effective
proterogynous forms, and polygamy suggests way of minimizing the deleterious consequences
that the size-advantage model is preferable, of drift and related phenomena in small, iso-
although a gene dispersal effect is possible. lated populations. Both versions predict modi-
fications in the sexual system, wherever a change
SUMMARY AND CONCLUSIONS in ecology reduces gene flow between the com-
ponent populations of a species.
An animal's reproductive apparatus is
adapted so as to maximize the probability that ACKNOWLEDGMENTS
the individual's genetic material will be incor-
In developing the exposition of these ideas, the
porated into that portion of the next genera-
advice and criticisms of the following persons, who
tion which will reproduce. What constitutes take no responsibilityfor errors,were most helpful:
such adaptation depends not only upon the G. W. Barlow, R. D. Beeman, C. W. Birky, Jr.,
individual's capacity for interacting with J. H. Brumbaugh,W. Z. Lidicker,T. J. M. Schopf,
another member of its species and with its en- P. C. Schroeder,G. L. Stebbins and J. Tomlinson.

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A Hipótese Da Vantagem Do Tamanho

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The Evolution of Hermaphroditism Among Animals

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INTRODUCTION We may also dismiss the Lamarckian notion

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