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Journal of Heredity 2010:101(Supplement 1):S100–S106
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Male Sex Drive and the Maintenance of
Sex: Evidence from Drosophila
RAMA S. SINGH
AND
CARLO G. ARTIERI
From the Department of Biology, McMaster University, Hamilton, Ontario, Canada L8S4K1. Carlo G. Artieri is now at the
Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases,
National Institutes of Health, US Department of Health and Human Services, Bethesda, MD 20892.
Address correspondence to Rama S. Singh at the address above, or e-mail: [email protected].
Abstract
The resolution of the paradoxes surrounding the evolutionary origins and maintenance of sexual reproduction has been
a major focus in biology. The operation of sexual selection—which is very common among multicellular organisms—has
been proposed as an important factor in the maintenance of sex, though in order for this hypothesis to hold, the strength of
sexual selection must be stronger in males than in females. Sexual selection poses its own series of evolutionary questions,
including how genetic variability is maintained in the face of sustained directional selection (known as the ‘‘paradox of the
lek’’). In this short review, we present evidence obtained from recent comparative genomics projects arguing that 1) the
genomic consequences of sexual selection clearly show that its effect is stronger in males and 2) this sustained selection over
evolutionary timescales also has an effect of capturing de novo genes and expression patterns influencing male fitness, thus
providing a mechanism via which new genetic variation can be input into to male traits. Furthermore, we argue that this
latter process of genomic ‘‘masculinization’’ has an additional effect of making males difficult to purge from populations, as
evidence from Drosophila indicates that, for example, many male sexually selected seminal fluid factors are required to ensure
maximally efficient reproduction. Newly arising parthenogenic mutations would suffer an immediate reproductive rate
disadvantage were these proteins lost. We show that recent studies confirm that genomic masculinization, as a result of
‘‘male sex drive,’’ has important consequences for the evolution of sexually dimorphic species.
Key words: maintenance of sex, male biased genes, male sex drive, rapid evolution, sexual selection
Few other topics, barring selection and adaptation, has
attracted the level of attention that evolutionary biologists
have lavished on the evolution of sex. The near ubiquity of
sexual reproduction in multicellular organisms suggests that
it may be linked with their success; however, the origin and
evolution of sexual reproduction remains a mystery. Why
should a population tolerate a large proportion of males
(typically 50%), individuals who often contribute nothing
more than gametes to the act of reproduction? Males’
contribution via gametes is miniscule compared to the
resources they consume, and, in theory, a mutation allowing
females to reproduce asexually should sweep through the
population as an asexual population would benefit from
twice the reproductive rate; a concept that Maynard-Smith
(1978) termed as the 2-fold cost of sex (or alternatively, the
cost of males). The problem of sex— that is, its origin and
maintenance—has been at the center of evolutionary
biology since the mid-1970s and volumes have been written
about it (e.g., Maynard-Smith 1978; Bell 1982). As the origin
of sex is embedded in the same pre-Cambrian antiquity as
the origin and evolution of multicellularity, it has attracted
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relatively less attention than its maintenance, though the
reigning theory is that sex evolved as a by-product DNA
repair mechanisms (Bernstein et al. 1985, but see Margulis
and Sagan 1990).
The maintenance of sex, being much more tractable to
experimentation, has garnered much attention among
population geneticists and a host of hypotheses regarding
how sexual reproduction is maintained —or how the 2-fold
cost of sex is ‘‘paid’’—have been proposed (reviewed in
Butlin 2002). These hypotheses generally fall into 2 broad
camps: either sex is advantageous because it increases the rate
of adaptive evolution by reshuffling genotypes and maintaining additive variation, as epitomized in the classic ‘‘Red
Queen’’ hypothesis (Van Valen 1973; Jaenike 1978; Hamilton
1980; Bell 1982), or sex is more efficient at purging
deleterious mutations, as exemplified in Kondrashov’s
‘‘deterministic mutation’’ hypothesis (Kondrashov 1988). In
addition, it has also been suggested that no single mechanism
may explain the prevalence and maintenance of sex but rather
that combinations of the various hypotheses may act
synergistically (West et al. 1998). Another somewhat different
Singh and Artieri Masculinization and the Maintenance of Sex
approach for explaining the maintenance of sex is to find
situations wherein its cost is reduced: the 2-fold cost is
predicated on the assumption that males contribute nothing
more than gametes (Maynard-Smith 1978). For instance,
there have been numerous attempts made to find examples
where males make contributions beside gametes, such as
nuptial gifts in insects and parental care in birds and in
mammals (Andersson 1994). Although these instances
illustrate cases wherein males make significant contributions
to reproduction, they involve taxon specific ecological
situations, and thus are unsuitable as a general mechanism
explaining the maintenance of sexual reproduction (see
Meirmans and Neiman 2006). Finally, a yet another approach
goes further in terms of disassociating the origins of sexual
reproduction from its maintenance. Ignoring the question of
the origins of sexual reproduction, this line of reasoning
makes use of the argument that once sex evolves it is difficult
to eliminate (see Engelstädter 2007 for review). Under such
hypotheses, it is argued that once the specific cellular,
physiological, and genetic systems underlying sexual reproduction have evolved to require the input of both parents,
it is difficult for a mutation causing asexual reproduction to
arise and reach an appreciable frequency in the population in
the first place. For example, it has been shown in a variety of
species that male gametic factors are required in order to initiate
embryonic development (e.g., Stricker 1999; Manandhar et al.
2005) and have presumably evolved in order to prevent cell
cycle arrest due to unfertilized eggs having only a haploid
chromosome complement. Thus in order for asexuality to
evolve, these physiological ‘‘checkpoints’’ would first have
to be obviated. Although this does not make reversion to
asexuality in a sexual lineage impossible, it increases the number
of evolutionary ‘‘steps’’ required to complete the process, the
intermediates of which are frequently expected to show
reduced fitness (Engelstädter 2007).
There has been very little attention given to the
possibility that the process of reproduction itself, rather
than its consequences in terms of generation and modulation of variation, may have a role to play in the maintenance
of sex. Sexual selection is a common feature of higher
organisms, particularly insects, birds, and mammals, and
although it cannot explain the origins of sexual reproduction, recent hypotheses have suggested that it may be
involved in its maintenance. For instance, Agrawal (2001)
and Siller (2001) proposed that if the deleterious phenotypic
effects of mutation are stronger in males than in females, the
higher reproductive variance of males as compared with
females will allow them to act as a sieve through which
deleterious mutations are purged, leading to an increase in
overall population fitness. More recently, Whitlock and
Agrawal (2009) have reexamined this hypothesis and argued
that the condition dependence that is often observed in the
case of male traits (i.e., the association of the strength of
their expression with overall male genetic condition)
increases the likelihood that deleterious mutations will have
a stronger negative effect on male—rather than female—
reproductive fitness; deleterious mutations will likely decrease male condition and thus reduce their success rate in
intrasexual competition. However, this reformulated argument requires that sexual selection has a stronger effect on
males than females; a situation that the authors claim that
there ‘‘are almost no data available to address.’’
In this short review, we build on the data that were
previously used in order to propose the theory of male sex
drive (MSD) (Singh and Kulathinal 2005) or the elevated
effect of sexual selection on males due to male–male
competition and their interest in overcoming female
resistance. Furthermore, we argue that the inherent interest
of males in producing the maximum number of possible
offspring may lead to a situation wherein a greater number
of offspring, and hence reproductive rate, is achieved in
sexual as compared with asexual systems. Recent evidence
collected from the fields of speciation and comparative
genomics have revealed a pronounced pattern of genomic
‘‘masculinization’’ or the observation that a greater proportion of the genome is involved in male-specific function
as compared with female-specific function or expressed at
higher levels in males. This results from the capture of new
male-biased expression patterns, mutations in existing
genes, as well as de novo genes—via processes such as
duplication and retrotransposition—that assist in the ability
of males to secure copulation. This pattern of masculanization provides ample support for the notion that selection is
stronger in males than in females and also suggests
a mechanism by which the amount of heritable genetic
variation associated with male traits is increased, reducing
the difficulties associated with the ‘‘lek paradox,’’ or the
expected depletion of heritable additive genetic variation in
the face of strong directional selection (Borgia 1979).
Although our discussion will focus mainly on Drosophila,
several recent analyses have extended the observations
made in fruit flies to a number of different organisms, and
we will note these when appropriate.
Rapid Male Evolution
Early 2-dimensional gel electrophoresis studies noted that
proteins expressed in the male reproductive tract showed
greater intra- and interspecific divergence in Drosophila
species in comparison with female or nonreproductive
proteins (Coulthart and Singh 1988; Civetta and Singh
1995). These observations were confirmed at the nucleotide
coding sequence level using reproductive and nonreproductive genes in a number of species groups including Drosophila
(Civetta and Singh 1998), abalone (Swanson and Vacquier
1995), Caenorhabditis (Reinke et al. 2004; Artieri et al. 2008),
and mammals (Torgerson et al. 2002) (reviewed in Swanson
and Vacquier 2002). Furthermore, the recent increase in the
application of large-scale sequencing has extended these
observations to both the genomic and transcriptomic levels.
Haerty et al. (2007) used the recently released full sequences
of 12 Drosophila species (Drosophila 12 Genomes Consortium 2007) in order to examine patterns of sex and
reproduction related (SRR) gene evolution, both male
and female, relative to nonsex genes. Genes with known
male-specific function or known to be expressed in male
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tissues (see below) were shown to evolve significantly more
rapidly than female-specific or nonsex genes. In addition,
genes expressed in the female reproductive tract (but not the
ovary) were significantly more conserved than nonsex genes.
Furthermore, the study noted that genes involved in male
reproductive function were significantly less likely than
female or nonsex genes to share identifiable orthologs
among the 12 species examined, indicating either that these
genes are so diverged that orthology cannot be unambiguously assigned or that there is an overrepresentation of
lineage-specific, de novo genes among those with male
function (Haerty et al. 2007; see below).
In addition to their rapid evolution at the coding
sequence level, several studies have shown that male genes
evolve more rapidly at the level of gene expression as well
(reviewed in Ellegren and Parsch 2007). The first studies to
examine the dynamics of sex-biased gene expression, that is,
genes that are expressed at elevated levels in one sex relative
to the other, in Drosophila noted that male-biased genes
(MBGs) show more expression polymorphism within
species (Meiklejohn et al. 2003), and divergence between
Drosophila melanogaster and D. simulans (;2.5 million years
diverged [MYD]) than female-biased genes (FBGs) or
unbiased genes (Ranz et al. 2003). These results were
questioned, however, due to the possibility that they were an
artifact of having used a D. melanogaster microarray to
measure expression levels in D. simulans, without the use of
appropriately stringent specificity thresholds (see Gilad et al.
2005). Nevertheless, the accelerated rate of divergence of
MBGs was subsequently confirmed in a larger scale study of
7 Drosophila species using species-specific microarrays
(Zhang et al. 2007). Not only did this study note that
MBGs were more diverged at both the transcriptome and
coding sequence levels but also that in most species,
a significantly greater fraction of the genome is male-biased
as compared with female-biased (see below). This pattern of
rapid evolution of MBG expression is not restricted to flies,
and similar patterns have been observed in humans
(Khaitovich et al. 2005) and mice (Voolstra et al. 2007).
The Masculinized Genome
The remarkable patterns of evolution seen in male-biased
and male-specific genes are not confined to the level of
accelerated divergence between species; in addition, evidence continues to accumulate attesting to the notion that
the genomes of sexual species are being reorganized in such
a way that male genes are located in favorable positions and
also that an overall greater proportion of genes are involved
in male function (Singh and Kulathinal 2005). For instance,
a number of recent studies have found a paucity of MBGs
on the X chromosome in Drosophila (Parisi et al. 2003; Ranz
et al. 2004; Sturgill et al. 2007), mammals (Emerson et al.
2004), and Caenorhabditis (Reinke et al. 2000; Artieri et al.
2008). These observations were originally found to be
puzzling as theory had predicted that in XY systems, newly
arising, recessive male-beneficial mutations would be favored
on the X, especially if these mutations produced an
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antagonistic effect in females. Such mutations are directly
exposed to selection in hemizygous males and will not
experience strong counterselection in females until they reach
a significant frequency in the population (Charlesworth et al.
1987). If, however, male-beneficial mutations tend to be at
least partially dominant (d . 0.5), they will be favored on
autosomes: each X chromosome spends two-third of its time
in females and thus selection for male-specific traits will
experience reduced efficiency. The overwhelming pattern
observed in the genomic data is thus suggestive of positive
selection acting to maintain at least partially dominant malebeneficial mutations (see below).
The idea that a larger proportion of the genome is
involved in male-specific function had been suspected long
prior to the advent of genomics as several decades worth of
data from mutation screens and introgression studies had
shown a consistent bias toward a larger number of genes
whose mutation produced male sterile as compared with
female-sterile phenotypes (e.g., Lindsley and Lifschytz 1972;
Hollocher and Wu 1996; True et al. 1996; Masly and
Presgraves 2007). These observations were also supported
via the work of expression studies, which, as noted above
revealed that the majority of Drosophila species show
a significant bias toward a larger number of genes with
male-biased expression (Zhang et al. 2007). This may be
largely due to the effect of the testes deploying a larger
number of unique genes when compared with the ovary
(Parisi et al. 2003). In addition and as noted above, the
availability of whole genome sequences has revealed that
genes involved in male-biased and male-specific functions
experience an increased rate of turnover (Haerty et al. 2007;
Zhang et al. 2007). Although there is abundant evidence of
lineage-specific acquisition of genes affecting male function
from a variety of different systems (e.g., Durand et al. 2006;
Haerty et al. 2007; Krzywinska E and Krzywinski J 2009),
we will focus on one well-studied group of genes in
Drosophila: the accessory gland proteins (acps), which
illustrate many of the concepts raised in this review.
Acps are the product of the male accessory glands,
paired structures located adjacent to the testes in the insect
abdomen. These glands contain secretory tissue that is
responsible for producing a number of products that are
added to the male’s ejaculate via their attachment to the
ejaculatory duct (for a recent review of the accessory glands
and their products see Ram and Wolfner 2007). It has long
been known from transplantation studies that the products
of the accessory glands have direct physiological effects on
females (Garcia-Bellido 1964; Merle 1968). Using modern
genomic technology, more than 100 distinct acps have been
identified in Drosophila whose effects in females include
decreasing their attractiveness to males, decreasing their
receptivity to mating, elevating their egg-laying rate, and
increasing their rate of sperm storage (Wolfner 1997). The
overall commonality among acp function is that the vast
majority of those characterized have the net effect of
enhancing male reproductive success (Wolfner 1997).
Consonant with the idea that acps are the product of sexual
selection and competition acting to increase male
Singh and Artieri Masculinization and the Maintenance of Sex
reproductive success and overcome female resistances, acps
are among the most rapidly evolving MBGs—thus making
them among the most rapidly evolving genes in the fly
genome (Haerty et al. 2007; Ram and Wolfner 2007).
Perhaps even more intriguing than their rapid rate of
evolution, acps appear to be subject to frequent lineagespecific gene acquisition. For instance, in their analysis of
genomic patterns of divergence in SRR and nonsex proteins,
Haerty et al. (2007) noted that .97% of female reproductive
tract genes had identifiable 1:1 best reciprocal hit orthologs in
comparisons as distant as that between D. melanogaster and
D. grimshawii (;60 MYD; Tamura et al. 2004). In contrast,
,50% of male seminal fluid proteins had identifiable
orthologs in the same comparison. Therefore, as is the case
for other genes involved in male function, acps experience
not only accelerated evolution but also increased rates of
lineage-specific acquisition via processes such as tandem
duplication, retrotransposition, and de novo generation. De
novo generation of acps is likely rather rare, and it is likely
that generation of male-specific paralogs via various
mechanisms of gene duplication play a disproportionate role
in this process. Finally, acps are not found only in insects but
rather appear to be the result of a phenomenon applicable to
all sexual taxa; evidence for their rapid evolution also exists in
primates, for example (Clark and Swanson 2005).
What Drives Rapid Evolution and Masculinization?
Although the patterns of rapid evolution observed in male
genes are interesting in their own right, the more significant
question remains, ‘‘what drives the more rapid evolution of
MBGs as compared FBGs?’’ The 3 most popular hypotheses
are 1) relaxed selective constraint, 2) adaptation via sexual
conflict, or 3) adaptation via sexual selection. Relaxed selective
constraint in male proteins may occur via 2 nonmutually
exclusive mechanisms. First, male systems may simply be less
sensitive to perturbation, and thus tolerate a larger number of
partially deleterious nonsynonymous substitutions, leading to
the elevated dN/dS ratios observed in these genes. However,
this would appear to contradict the observation that male
reproductive functions are more sensitive to perturbation in
mutagenesis or introgression experiments (Wu and Davis 1993;
Singh and Kulathinal 2005). Second, male-limited expression of
MBGs reduces the efficacy of selection (see above), and thus
divergence could accumulate ‘‘neutrally’’ in females (Wade
1998; Cruickshank and Wade 2008; Morrow et al. 2008).
Although it is quite likely that this process is taking place,
a similar process should be occurring on autosomal FBGs, and
yet we do not observe the widespread rapid evolution of female
genes. Consequently, it would appear that relaxed selective
constraint cannot account for the genome-level patterns that
we observe.
In contrast, there appears to be extensive evidence that
the increased rate of divergence occurring in many of the
genes involved in male reproductive function show
evidence of having been driven by positive selection
(Civetta and Singh 1999; Singh and Kulathinal 2000;
Swanson and Vacquier 2002; Pröschel et al. 2006). For
instance, ;36% of identified acps show evidence of having
been subjected to recent positive selection (Swanson et al.
2001; Mueller et al. 2005; Haerty et al. 2007). A plausible
mechanism driving the accelerated evolution of acps is
sexual conflict or the coevolutionary arms race between the
sexes in the attempt to force each other to reproduce at
opposing reproductive optima (see Arnqvist and Rowe
2005 for extensive review). Under this scenario, males
evolve strategies, such as acps, that force females to
reproduce above their own optimal rate, whereas females
evolve counteradaptations in order to favor their own
reduced optimum. Although evidence for sexual conflict is
persuasive and continues to accumulate (e.g., Arnqvist and
Rowe 2005; Hall et al. 2008), the simple observation that
we do not see a similar pattern of accelerated evolution in
female genes would appear to rule out the possibility that
sexual conflict is the dominant driver of male evolutionary
change (Civetta and Singh 2005; Kulathinal and Singh
2008). This, of course, assumes that both sides of the
conflict involve mutations occurring in similar underlying
genetic architectures. If, however, adaptations occurring in
females that confer resistance to males generally require
fewer mutational steps, then conflict could explain the
excess of rapid male evolution. Barring such a situation, the
most plausible driver of rapid divergence of genes associated
with male function is a combination of intersexual conflict
and traditional Darwinian notions of sexual selection, with
special emphasis placed on male–male competition, especially
in the form of sperm competition.
MSD Theory and the Input of Variation
MSD can be defined as the differential/elevated effects of
all actions performed by the male, as compared with the
female, during mating—from the start of the search for
mates to the beginning of the next mating cycle (Singh and
Kulathinal 2005). This will include, but is not limited to,
male–male competition, searching for mates, vigorous
display and courting, mating and copulation duration,
sperm quantity and quality, mate guarding, and readiness
for remating. The MSD theory is based on the assumption
that sexual selection is stronger in males as compared with
females (except, of course, where in cases the sexual role is
reversed), which can be seen among males in all aspects of
mating as noted above. Darwin noted the heightened
expression of sexual selected traits in the male and
remarked ‘‘males with their superior strength, pugnacity,
armaments, unwieldy passion and love songs, are almost
always the more active and most often, the initiators of
sexual interactions’’ (Darwin 1871). Being preoccupied
with providing explanations for individual traits, Darwin
was not able to see overall, long-term consequences of
stronger sexual selection in males. Effectively, MSD is the
result of elevated sexual selection in the male over the
female and can therefore be expressed as ‘‘male-biased
sexual selection’’—of course, it also includes the effect of
sexual and natural selection. MSD provides an explanation
for the unique genomic features observed in males and acts
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as a contrast to such features being the result of female
choice.
Traditionally, the presence of sustained directional
selection as is observed in males of species subject to
strong sexual selection would be expected to deplete
additive genetic variation, leading to fixation of particular
male traits (Crow 2008). However, if such were the case, it
would no longer be in the interest of females to be choosy.
The lack of male variability would preclude selected traits
from being a reliable indicator of mate quality: a situation
that has been called the paradox of the lek (Borgia 1979;
Andersson 1994). And yet, females continue to choose;
thus an integral subject of recent interest in the field of
sexual selection has been to explain how such variability is
maintained. One particularly promising avenue of investigation has been to suggest that male traits provide an
especially large mutational target such that sufficient
variability can be maintained at mutation–selection balance
(see Tomkins et al. 2004 for review). Within this
framework, much attention has been paid to the ‘‘genic
capture hypothesis’’ (Rowe and Houle 1996), which
suggests that male traits are often condition-dependent.
This means that the strength of their overall expression is
determined by overall genetic condition, and thus is subject
to the input of a large proportion of the genome.
Therefore variation at a great many genomic loci inputs
into the overall variability of the male trait and trait
variability is maintained even in the face of strong
directional selection. Evidence for the genic capture
hypothesis is abundant and it almost certainly plays
a significant (if not predominant) role in resolving the lek
paradox (Tomkins et al. 2004; Arnqvist and Rowe 2005).
Nevertheless, we wish to suggest that the MSD
hypothesis, via sustained directional selection, provides
another avenue via which male traits may be expected to
provide an especially large mutational target (Singh and
Kulathinal 2005). As noted in the numerous examples
presented above, the genomes of sexually selected taxa are
becoming progressively masculinized, including a larger
proportion (acompared to females) of genes involved in
male reproductive traits, a larger proportion of genes
expressed at higher levels in males, and also a larger number
of male lineage-specific de novo genes. Each of these
examples indicates that the genome is dynamic and that
male traits may present a larger mutational target because,
over evolutionary timescales, selection will favor the
retention of any novel genes (duplications, retrotranspositions, exonization, etc.) or expression patterns that are
beneficial to males, consequently increasing the overall
proportion of the genome affecting male traits under
selection. Our example of the acps in Drosophila illustrates
the notion that strong directional selection leads to an
increase in lineage-specific acquisition of functional paralogs
and de novo genes. Even in the case of sexually selected
nondisplay traits, such as those involved in sexual conflict
scenarios, which should not be expected to be subject to
condition dependence, variability may be maintained via
mechanism outlined in MSD.
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Implications for the Maintenance of Sex
Finally, we wish to suggest that the net effect of increased
sexual selection in males may foster a situation wherein
males are difficult to eliminate, thus favoring the maintenance of sex in the face of invasion from asexuals. MSD
posits that genomic masculinization occurs due to strong
selection pressure favoring the ability of males to secure
copulation by all means—via mating-related male–male
competition or male–female interaction—and induce females to reproduce at their maximum capacity, which even
goes so far as to involve acps that induce increased
ovulation, for example (Wolfner 1997). A typical assumption of sexual conflict theory has been that the female’s
mating rate is optimal, whereas the male’s is excessive. Thus,
such conflict may favor a situation wherein female’s mating
acceptance threshold is increased and can only be overcome
by zealous males. Although a classic paper in the field of
sexual conflict theory showed that experimental removal of
such competition via enforced monogamy led to higher
reproductive output (Holland and Rice 1999), such removal
of competition is impossible in nature. Thus, in the short
term, removal of male input into mating may lead to an
overall reduced reproductive output. Also, as noted above, it
has been determined that in many species, male gamete- and
seminal fluid-specific factors are required in order to ensure
proper fertilization (beyond the obvious contribution of
one-half the total 2n genomic complement) (see Engelstädter
2007 for review). Under MSD, such factors will be favored
if they increase the success rate of male fertilization or
increase the total number of progeny produced. These
factors, either in the gametes themselves or in the form of
acps, may initially be nonessential but, over evolutionary
time, become required to complete fertilization. A plausible
example of an intermediate step in such a process is the
ovulin acp in Drosophila that induces ovulation in females and
for which evidence suggests it mimics the female’s own egglaying hormones (Monsma and Wolfner 1998; Ram and
Wolfner 2007). By reducing the need for the presence of the
their own ovulation proteins, females could eventually
become dependent on the male’s acps in order to lay eggs at
an elevated rate. Thus, loss of the male’s input in the case
of a fictional, newly arising parthenogenesis mutation
would incur an immediate penalty in terms of a reduced
reproductive rate.
Conclusion
Our purpose in this short review has been 2-fold. First, we
have argued that the overall effect of this increased selection
pressure acting on males, which Singh and Kulathinal (2005)
have termed MSD, may have implications for both the
maintenance of genetic variation as well as for the
maintenance of sexual reproduction itself. Various lines of
evidence suggest that male-specific gene acquisition is
prevalent in sexually selected taxa and that this will increase
the mutational target of male-specific traits allowing the
continued input of heritable variation. Furthermore, the net
Singh and Artieri Masculinization and the Maintenance of Sex
effect of these male-driven sexual behaviors—physical,
physiological, and behavioral—is that MSD provides direct
benefits to reproducing pairs. This manifests itself in terms of
favoring elevated reproductive rates, perhaps ultimately
leading to a greater number of offspring being produced in
sexual versus asexual multicellular species, both making males
difficult to purge and perhaps assisting to compensate for the
2-fold cost of sex. Second, we have provided evidence from
the field of comparative genomics that sexual selection is
indeed stronger in males, thus consistent with Whitlock and
Agrawal’s (2009) hypothesis that sexual selection can
efficiently purge mutations from the population via the
higher reproductive variance in males. The hypotheses
proposed in this review suggest that the process of
reproduction itself, at the level of all interactions among
mating pairs, from mate choice to fertilization, and not simply
its long-term consequences, may play an important role in
explaining how and why sexual reproduction is maintained.
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Funding
Drosophila 12 Genomes Consortium. 2007. Evolution of genes and
genomes on the Drosophila phylogeny. Nature. 450:203–218.
Natural Sciences and Engineering Research Council of
Canada (NSERC) Post-Graduate Doctoral Scholarship (to
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Acknowledgments
The authors would like to thank Wilfried Haerty and Abha Ahuja, as well as
2 anonymous reviewers for helpful discussion on this topic.
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Received October 7, 2009; Revised January 5, 2010;
Accepted January 18, 2010
Corresponding Editor: John Logsdon