narios for the intermediate steps leading to the various
cases of derived life cycles and to describe the kinds
of evidence that would support or falsify these scenarios.
Limnadiinae
The largest number of deviations from gonochoric
reproduction occurs within the Limnadiinae (Table 1).
Although most of the examples of unisexual Eulimnadia in Table 1 are from North and South American
species, that pattern is more a function of the available data than a zoogeographic pattern of unisexuality.
Many of the Indian species are probably unisexual as
well, but quantitative data on large population samples
is unavailable (Radhakrishna & Durga Prasad, 1976).
Female-biased populations of Eulimnadia are found
throughout the world. Limnadia populations are usually either unisexual or gonochoric (Table 1) although
cases of female bias are known.
The taxonomic relationships of limnadiinine genera are unclear. Sars (1896b) suggested that Australian
species of Limnadia, differing in their reproductive
modes from other congeners, could be allocated into a
new genus, Paralimnadia Sars. Thus, the three genera
of Limnadiinae would tend to differ in their characteristic sex ratios: Paralimnadia having male:female
equality; Eulimnadia having female-bias ranging to
male absence; and Limnadia (narrowly defined) being
unisexual. He later modified his interpretation of sexuality in Limnadiinae (Sars, 1902) by suggesting that
Paralimnadia was a transitional group between obligately sexual and unisexual Iimnadiids, with Limnadia
being completely unisexual. He viewed Eulimnadia
also as reproducing completely by unisexual means,
but with rare males representing the expression of
atavistic traits and themselves playing no role in the
reproductive biology of these species. Both of Sars'
inferences (1986b; 1902) would suggest the existence
of a phylogenetic imprint to sex ratio variation in Limnadiinae.
Sars' concept of Paralimnadia has not survived
the test of time and many of the distinctions between
Limnadia and Eulimnadia have become blurred over
the years. Although most modern authors distinguish
between these two genera (Belk, 1989; Martin, 1989;
Roessler, 1990, 1991a, 1994a, b), Webb & Bell
(1979) have argued that they are synonymous, and
some authorities concur (Cesar, 1990). Yet efforts to
establish diagnostic characteristics for their separation
57
have not been definitive (for a review, see Straskraba,
1965a).
The nature of the reproductive system in Eulimnadia texana provides an alternative way of explaining
sex ratio evolution in Limnadiinae. Female-biased and
unisexual life cycles in this group are explicable as
population genetic consequences of the basic androdioecious life cycle (Fig. 2B). Suppose that the ancestor
of current androdioecious species was an obligately
sexual limnadiid with a system of sex determination
involving female heterogamety (Fig. 2A). The origin of androdioecy requires only the differentiation of
parts of the gonads of females to be sperm-producing
(i.e., the transition from ovary to ovotestis). Simultaneous hermaphroditism is a common attribute of the
lower crustaceans. It has been found in Cephalocarida (Hessler et ai., 1970) and in Remipedia (Ito &
Schram, 1988) and has long been known in notostracans (reviewed in Sassaman, 1991). In the nonbranchiopod crustacean groups, the testicular tissue
is usually confined to a different pair of gonadal lobes
than the ovarian tissue, and sometimes opens via a separate gonoduct. In these cases it is presumed that fertilization requires pairing of two individuals and involves
reciprocal outcrossing. In notostracans (Longhurst,
1955) and conchostracans (Zaffagnini, 1969) the testicular tissue is interspersed with ovarian tissue so that
gametes can mingle within a common oviduct to allow
selfing.
The evolutionary transition to self compatibility
alone is sufficient to initiate androdioecy, a state from
which unisexuality is one alternative populational consequence. The evolutionary dynamics of the androdioecious system in E. texana has been modeled with
explicit mathematical theory (Otto et ai., 1993). A
polymorphic equilibrium, in which males and both
monogenic and amphigenic females are retained in the
population, occurs when there is high male fitness or
high inbreeding depression associated with predominantly selfing reproduction, or both. When neither is
high, the system rapidly evolves to unisexuality, which
is a boundary state of fixation on the S allele. Evolution of population sex ratio from a state of male:female
equality to one of unisexuality is simply a population
genetic process operating on alternate alleles at the sexdetermining locus. Figure 3 illustrates the relationship
between the mode of reproduction, polymorphism at
the sex-determining locus, and population sex ratio in
this transitional process.
This view of the evolutionary dynamics of limnadiine species makes different predictions about system-
cases of derived life cycles and to describe the kinds
of evidence that would support or falsify these scenarios.
Limnadiinae
The largest number of deviations from gonochoric
reproduction occurs within the Limnadiinae (Table 1).
Although most of the examples of unisexual Eulimnadia in Table 1 are from North and South American
species, that pattern is more a function of the available data than a zoogeographic pattern of unisexuality.
Many of the Indian species are probably unisexual as
well, but quantitative data on large population samples
is unavailable (Radhakrishna & Durga Prasad, 1976).
Female-biased populations of Eulimnadia are found
throughout the world. Limnadia populations are usually either unisexual or gonochoric (Table 1) although
cases of female bias are known.
The taxonomic relationships of limnadiinine genera are unclear. Sars (1896b) suggested that Australian
species of Limnadia, differing in their reproductive
modes from other congeners, could be allocated into a
new genus, Paralimnadia Sars. Thus, the three genera
of Limnadiinae would tend to differ in their characteristic sex ratios: Paralimnadia having male:female
equality; Eulimnadia having female-bias ranging to
male absence; and Limnadia (narrowly defined) being
unisexual. He later modified his interpretation of sexuality in Limnadiinae (Sars, 1902) by suggesting that
Paralimnadia was a transitional group between obligately sexual and unisexual Iimnadiids, with Limnadia
being completely unisexual. He viewed Eulimnadia
also as reproducing completely by unisexual means,
but with rare males representing the expression of
atavistic traits and themselves playing no role in the
reproductive biology of these species. Both of Sars'
inferences (1986b; 1902) would suggest the existence
of a phylogenetic imprint to sex ratio variation in Limnadiinae.
Sars' concept of Paralimnadia has not survived
the test of time and many of the distinctions between
Limnadia and Eulimnadia have become blurred over
the years. Although most modern authors distinguish
between these two genera (Belk, 1989; Martin, 1989;
Roessler, 1990, 1991a, 1994a, b), Webb & Bell
(1979) have argued that they are synonymous, and
some authorities concur (Cesar, 1990). Yet efforts to
establish diagnostic characteristics for their separation
57
have not been definitive (for a review, see Straskraba,
1965a).
The nature of the reproductive system in Eulimnadia texana provides an alternative way of explaining
sex ratio evolution in Limnadiinae. Female-biased and
unisexual life cycles in this group are explicable as
population genetic consequences of the basic androdioecious life cycle (Fig. 2B). Suppose that the ancestor
of current androdioecious species was an obligately
sexual limnadiid with a system of sex determination
involving female heterogamety (Fig. 2A). The origin of androdioecy requires only the differentiation of
parts of the gonads of females to be sperm-producing
(i.e., the transition from ovary to ovotestis). Simultaneous hermaphroditism is a common attribute of the
lower crustaceans. It has been found in Cephalocarida (Hessler et ai., 1970) and in Remipedia (Ito &
Schram, 1988) and has long been known in notostracans (reviewed in Sassaman, 1991). In the nonbranchiopod crustacean groups, the testicular tissue
is usually confined to a different pair of gonadal lobes
than the ovarian tissue, and sometimes opens via a separate gonoduct. In these cases it is presumed that fertilization requires pairing of two individuals and involves
reciprocal outcrossing. In notostracans (Longhurst,
1955) and conchostracans (Zaffagnini, 1969) the testicular tissue is interspersed with ovarian tissue so that
gametes can mingle within a common oviduct to allow
selfing.
The evolutionary transition to self compatibility
alone is sufficient to initiate androdioecy, a state from
which unisexuality is one alternative populational consequence. The evolutionary dynamics of the androdioecious system in E. texana has been modeled with
explicit mathematical theory (Otto et ai., 1993). A
polymorphic equilibrium, in which males and both
monogenic and amphigenic females are retained in the
population, occurs when there is high male fitness or
high inbreeding depression associated with predominantly selfing reproduction, or both. When neither is
high, the system rapidly evolves to unisexuality, which
is a boundary state of fixation on the S allele. Evolution of population sex ratio from a state of male:female
equality to one of unisexuality is simply a population
genetic process operating on alternate alleles at the sexdetermining locus. Figure 3 illustrates the relationship
between the mode of reproduction, polymorphism at
the sex-determining locus, and population sex ratio in
this transitional process.
This view of the evolutionary dynamics of limnadiine species makes different predictions about system-