Prospects & Overviews
Problems & Paradigms
Are old males still good males and can
females tell the difference?
Do hidden advantages of mating with old males off-set costs related to fertility,
or are we missing something else?
Sheri L. Johnson and Neil J. Gemmell
Sperm function generally declines with male age.
Paradoxically, females of many species still choose to
mate with old males rather than young males. Females
choosing old mates may suffer reduced fertilization rates
and an increased incidence of birth defects in offspring,
lowering fitness which may in turn lead to conflict
between the sexes. This apparent paradox has generated much interest from theorists, but whether this
paradox presents in nature remains equivocal. Empirical
studies have found mixed support for both a decline in
fertility with male age and age-based female mate
preference. Here, we examine recent evidence for this
paradox, identify confounding variables, highlight areas
that deserve further investigation, and suggest avenues
for future research.
.
Keywords:
female mate preference; fertility; male age; mating history;
sperm traits
DOI 10.1002/bies.201100157
Centre for Reproduction and Genomics, Department of Anatomy,
University of Otago, Dunedin, New Zealand
*Corresponding author:
Sheri L. Johnson
E-mail: sheri.johnson@otago.ac.nz
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
Introduction
It is well known that female age significantly influences fertility [1, 2]. While less well studied, accumulating evidence
indicates that male age also affects fertility [3–6]. In humans,
numerous studies show age-related declines in semen volume,
sperm motility, and the proportion of morphologically normal
sperm [3, 7, 8], which are associated with reduced pregnancy
rates [2], increased pregnancy-associated complications and
potentially higher rates of birth defects in offspring [4–6, 9].
Age-related reductions in sperm quantity and quality (hereafter sperm traits), fertilization success, and offspring fitness
are also observed in invertebrates and other vertebrates
(Tables 1 and 2), suggesting that this is a general phenomenon.
Paradoxically, females of many species mate with old
rather than young males ([10–12], Table 2). In humans, women
prefer older mates than themselves, a pattern that appears to
be culturally universal [13] and likely related to resource
acquisition [13, 14]. Non-human mating systems can also be
resource based [15], but in many systems, males may contribute nothing more than sperm to a mating [16]. Some models of
age-related mate choice predict female preference for older
males, as older males have proven their high genetic quality
by surviving [11, 17]. Ironically, such a preference may have a
significant cost to female fitness; deleterious germline
mutations can accumulate in older males [18–20], rendering
older males, or at least their sperm, of lower genetic quality
than that of younger males [16, 19–21].
A large body of work, theoretical and empirical, has
attempted to understand this paradox ([10]; Fig. 1 and
Table 2). Our understanding of the age-related patterns of
sperm function decline and the mechanisms responsible are
almost entirely based on knowledge from human studies,
which are often confounded by variables like female age
and abstinence time [3]. In contrast, our knowledge of how
age influences male reproductive success and female mate
preference mostly derive from animal systems, given the complexities of such studies in humans.
www.bioessays-journal.com
609
S. L. Johnson and N. J. Gemmell
Prospects & Overviews
....
Problems & Paradigms
Table 1. Summary of recent evidence investigating decline in sperm traits with age in non-humans
Species
Domestic fowl,
Gallus gallus domesticus
Barn swallows,
Hirundo rustica
Blue-footed booby,
Sula nebouxii
Tree swallow,
Tachycineta bicolor
Cricket,
Teleogryllus oceanicus
Hide beetle,
Dermestes maculatus
Bluegill,
Lepomis macrochirus
Guppy,
Poecilia reticulata
Zebrafish,
Danio rerio
Brown Norway rat,
Rattus norvegicus
Iberian lynx,
Lynx pardinus
Domestic dog,
Canis lupus familiaris
Baird’s Tapir,
Tapirus bairdii
Asian elephant,
Elephas maximus
Gazelles,
Gazella spp.
Age classes
1–8 years
Normal
DNA
Velocity Motility Concentration Volume morphology Viability damage Refs.
NS
#
[35]
1–6 years
NS
3–10 vs.
>10 years
2 vs. >2 years
NS
[37]
"
NS
[65]
[100]
5–35 days
"
[101]
1–13 weeks
NS
[36]
6 vs. 7 vs. 9 years
"
4–6 vs.
12–16 months
290 vs. 911 days
NS
NS
NS
3–24 months
#
#
2 vs. 3 vs. 4 years
<2 vs. 2–7 vs.
>7 years
2–21 years
10–19 vs. 23–43 vs.
51–70 years
667–5,042 days
NS
[102]
"
"
NS
[24]
"
[25]
#
[22]
[103]
NS
NS
NS
"
NS
NS
NS
#
NS
NS
NS
"
#
"
NS
NS
NS
NS
[34]
[104]
#
NS
[23]
"
[48]
# indicates decline with age; " indicates increase with age, NS indicates non-significant change with age.
Experimental manipulation in animal systems has been illuminating, but ultimately inconclusive. For instance, sperm
motility has been found to decline with age in some species
[22, 23], but sperm production is known to increase with age in
others [24, 25]. Likewise, female preference for older males is
confirmed in some studies [10, 26–28], while others observe no
age-based preference [24, 25] or even significant discrimination against older males [16, 29–31]. Surprisingly little work
has been undertaken that experimentally investigates: (i)
whether male fertility declines with age, (ii) what mechanisms
might be involved, and (iii) ultimately whether females can
differentiate among males that are more or less fertile in a
single experimental system. Here, we review the theoretical
and recent empirical literature that examines age-based
decline in fertility and age-based female mate preferences.
We identify key confounding variables and suggest avenues
for future research.
Sperm traits tend to decline with male age
Humans
A review of the literature in 2001 showed that semen volume,
sperm motility, and normal sperm morphology decline when
610
comparing men of 30 years to those aged 50 [3]. Most of those
earlier studies were conducted on men attending infertility
clinics [3]. More recent studies were conducted in healthy,
non-smoking populations and report similar declines in sperm
volume and sperm quality [7, 32]. Declines in sperm concentration are reported in some studies, but many do not report a
decline [3, 32]. A growing number of studies have also found
declines in DNA integrity or increases in DNA fragmentation
with increasing male age [8, 33]. While a formal meta-analysis
is missing, the general consensus is that increasing male age
tends to be associated with a decline in sperm traits.
Unfortunately, much of this literature is fraught with low
sample sizes or statistical problems arising from confounding
variables [3].
Non-humans
A number of studies have investigated the effects of age on
sperm traits in non-human taxa and have reported mixed
findings (Table 1). Sperm quality has been found to decline
with age in some species [22, 23], but other studies observe no
such decline [25, 34]. Likewise, sperm quantity has been found
to decrease in fowl [35], but found to increase in other taxa
[24, 25, 36]. The most comprehensive study thus far in birds,
on the barn swallow, found that sperm quality generally
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
....
Prospects & Overviews
S. L. Johnson and N. J. Gemmell
Table 2. Summary of recent evidence investigating the impact of male age on male mating success, fertilization success, offspring
fitness, and female mate preference in non-humans
Age classes
2–3 vs. 6–8 years
Mating
success
Ya
1 vs. 8 years
Oa
Fertilization
success
Yb
Offspring
fitness
Female
preference
Refs.
[35]
[89]
2 vs. >2 years
NS
[100]
3 vs. 4 vs. 5 years
NSb
[96]
4–6 vs. 14–15 months
NSb
NS
[24]
290 vs. 911 days
Y
NS
[25]
9 vs. 41 vs. 91 days
I
Ib
[79]
11 vs. 47 vs. 88 days
I
I
1–13 weeks
I
I
1 vs. 5 days
Y
Y
5 vs. 15 vs. 25 days
I
2 vs. 14 days
1–5 months
Y
2–3 vs. 17–18 vs. 32–33 days
O
2–3 vs. 46–47 days
O
NS
[30]
[36]
NS
[105]
I
I
[59]
NS
O
[26]
[90]
O
3–5 vs. 25 days
[27]
O
[106]
Y
[107]
5–7 vs. 15–17 days
O
O
[28]
0 vs. 3, 6 or 9 days
NS
NS
[74]
3 vs. 30 days
NS
[31]
4–8 vs. 30–40 days
Y
Virgin , (NS);
non-virgin , (Y)
NS
[60]
Y
[75]
10–12 vs. 48–50 days
Yb
Y
Y indicates higher success for young males; I indicates higher success for intermediate-aged males; O indicates higher success for old males;
NS indicates no difference between males.
a
Assayed using social groups and fertilization success.
b
Competitive fertilization trial.
c
Resource-based mating system.
decreased with increasing male age [37]. Conversely, older
male bushcrickets produced bigger spermatophores, which
contained more sperm and had higher nutritional value
[38]. One of the few studies to assay sperm traits over a male’s
lifetime found that, for fowl, sperm swimming velocity of
individual males did not decline with age, but semen transfer
and the total number of sperm ejaculated showed a nonsignificant decline with age [35].
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
Age-related declines in sperm traits may
reduce reproductive success and affect
offspring fitness
Despite strong arguments that sperm traits should be particularly vulnerable to aging [5], evidence for an age-dependent
decline in reproductive success is mixed ([35]; Table 2). There
611
Problems & Paradigms
Species
Domestic fowl,
Gallus gallus domesticus
Great bustards,
Otis tarda
Tree swallow,
Tachycineta bicolor
Sockeye salmon,
Onchorynchus nerka
Guppy,
Poecilia reticulata
Zebrafish,
Danio rerio
Hide beetle,
Dermestes maculatus
Hide beetle,
Dermestes maculatus
Hide beetle,
Dermestes maculatus
Seed weevil,
Callosobruchus maculatus
Cabbage beetle,
Colaphellus bowringic
Fruitfly,
Drosophila pseudoobscura
Fruitfly,
Drosophila montana
Fruitfly,
Drosophila bipectinata
Fruitfly,
Drosophila bipectinata
Fruitfly,
Drosophila melanogaster
Thornbu treehoppers,
Umbonia crassicornis
European corn borer,
Ostrinia nubilalisc
Bulb mite,
Rhizoglyphus robini
Bulb mite,
Rhizoglyphus robini
Field cricket,
Gryllus bimaculatus
S. L. Johnson and N. J. Gemmell
Prospects & Overviews
....
Problems & Paradigms
Figure 1. Potential explanations argued to influence age-based female mate preference.
Boxes in bold are resource based arguments
(direct benefits).
is also a clear lack of studies that specifically investigate the
influence of sperm traits on fertilization success and offspring
fitness.
Fertilization success declines with male age
In humans, the pregnancy rate in couples where the male is
older than 35 years is 50% lower than in couples where the
male is less than 30, and the time to conception for the female
partner can be fivefold longer with men older than 45 years,
when compared to 25 year old men (reviewed in ref. [3]).
Likewise, advanced paternal age has been shown to have
negative long-term effects on reproductive fitness in mice
[55, 56]. In general, fertilization success does not appear to
increase with male age, as none of the studies listed in Table 2
document a fertilization advantage for older males.
Few studies have directly measured the relationship
between sperm traits and fertilization success. A recent study
in humans demonstrates that in vitro fertilization rates
decrease as sperm DNA fragmentation increases [57], a
parameter that is strongly concordant with male age [33].
Sperm transfer and the number of eggs laid is associated with
male age in the male hide beetle, with fertilization success
correlated with the number of sperm transferred [36].
Likewise, older male fowl tend to ejaculate sperm of lower
swimming velocity and fertilization success declines sharply
with age [35]. In contrast, old male guppies tend to produce
slower-swimming sperm than younger males, but these differences do not translate into a fertilizing advantage for younger
males [24]. This inconsistency might be due to a post-copulatory inbreeding avoidance mechanism that has subsequently been identified in this species [58].
Offspring fitness declines with male age in some species,
but remains equivocal
In humans, increasing male age has been linked to an
increased risk of obstetric complications, miscarriage, and
offspring disorders (e.g. autism, Down’s syndrome, epilepsy,
and schizophrenia [6]). The influence of male age on offspring
fitness has only been assessed in a handful of non-human
612
studies over the past decade (Table 2), but increased paternal
age has been linked to: negative long-term effects on development, longevity, and behavior in mice [55, 56], reduced hatching in cabbage beetles [59], reduced offspring size in a
mealworm beetle [29], reduced fecundity in daughters of a
bulb mite [60]. On the other hand, male age had a positive
effect on egg viability in the ladybird beetle [61].
Fleetingly few studies have specifically assayed how any
potential decline in sperm traits with age might affect offspring viability. DNA damage in the male germline has been
hypothesized to increase the mutational load carried by the
embryo [19, 51, 62, 63]. In humans, embryo quality has been
shown to decrease as sperm DNA fragmentation, a trait linked
to male age, increases [57]. Likewise, paternal levels of DNA
damage in the sperm influence offspring mortality in a species
of gazelle [48]. In the blue-footed booby, juvenile recruitment
declines with increasing male age [64], and older males have
been shown to have more DNA lesions in the germline (Box 1;
[65]). In addition, other studies have demonstrated a sex bias
in the offspring produced with sperm following prolonged
sperm storage by female [66, 67]. An important consideration
for such studies is that males with good sperm quality may still
be at risk for fathering offspring with a genomic defect. For
example, genomic defects are generally not associated with
sperm trait measures, with the exception of sperm motility,
which is inversely correlated with DNA fragmentation [33].
Given the dearth of information, there is a clear need to
specifically assay how sperm traits influence various measures
of offspring fitness in non-human systems, with and without
sperm storage capabilities. Further, additional studies are
needed to assess the relationship between sperm traits and
DNA damage, particularly in non-human studies where
confounding variables (e.g. abstinence time, lifestyle) can
be more tightly controlled.
Female mate preference can be age-based
Whether females benefit or incur costs by mating with old
males has long been debated (Fig. 1). Earlier reviews have
examined the theoretical basis of female mate preferences
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
....
Prospects & Overviews
Box 1
The blue-footed booby, Sula nebouxii: A current hypothesis is that females might be able to use oxidative
dependent secondary sexual signals as cues of mate
quality to avoid pairing and mating with males that
suffer from oxidative damage to their germline [68]. In
the blue-footed booby, foot color is a sexually selected
trait that strongly influences reproductive success [69,
70]. Carotenoid dependent foot color declines with age,
suggesting that aging incurs deterioration in the expression of a male sexual signal: older males incapable of
being as attractive as younger males [71]. Furthermore,
this decline is related to previous reproductive effort:
males that did not breed displayed more colorful feet
than males that reproduced the year before [72].
Reduced foot color affects mate choice, increases the
probability of the male in question being left for a younger
individual [68], and reduces female investment in eggs
[69]. Longitudinal data from two cohorts from a longterm study indicate that, after an initial increase, reproductive success of males declines progressively with
age [70] and juvenile recruitment declines with increasing male age [64]. Finally, older males (>10 years), with
accumulated reproductive experience, have more DNA
lesions in the germline than middle-aged males [65].
Overall, the data suggest that male sexual attractiveness
starts to decline at middle age, and this decline is correlated with increasing germline damage in old males. By
choosing males with attractive feet, females might
reduce the probability of their progeny bearing damaged
DNA [65].
[10, 11, 17–19, 73]; hence, here we highlight the key points
only. Older males are generally suggested to be more valuable
mates if the ability to provide direct benefits to a female is
positively correlated with age (e.g. parental care, territorial
defense; reviewed in ref. [10]). However, preference for older
males has also been demonstrated, both empirically and
theoretically, in species in which there appear to be no such
direct benefits [10–12]. Some early models of age-related mate
choice predict that females can gain indirect benefits by preferring to mate with older males as mates because they have
demonstrated their viability through survival [11, 17, 73], and
are likely to carry fewer deleterious alleles [17], whereas
cohorts of young males include males whose viability has
not yet been fully tested [10]. An alternative explanation for
female preference for older males is that older males are more
honest signalers, revealing more information about their
inherent quality in their sexual displays. This hypothesis is
dependent on male displays and the differences in signaling
between quality classes increasing with male age, making
female choice more effective among older males [12]. Re-examination of these models predicts that females should evolve a
preference for younger or intermediate-aged males, assuming
an increase in the number of deleterious mutations in the
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
germline with age [16, 18, 19, 21]. Discrimination against older
males is predicted to be particularly strong in species where
females obtain only sperm from a mating and no other direct
benefits [16, 20, 21]. Finally, assessing the age of a potential
mate may not always be possible. It may simply be too costly
for females to resist mating [62], or females may avoid having
their eggs fertilized by males with reduced fertility by mating
with multiple males [5, 62], which may explain the lack of agebased preference in some studies (Fig. 1; Table 2).
Empirical evidence for age-based female mate
preference
Evidence relevant to the age-based viability indicator model
was reviewed in 2001 [10], leading to the conclusion that while
females mating with old rather than with young males might
receive indirect (genetic) fitness benefits under many circumstances, such benefits are not universal [10]. That earlier work
suggests that when male age is potentially correlated with
resources (e.g. paternal care or territory), females appear to
prefer to mate with old males [10]. However, when age is not
correlated with resources the evidence was more equivocal
[10]. Studies in the intervening decade have mostly been
conducted in non-resource based systems and have been
equally equivocal, identifying preferences spanning old,
young, and middle-aged males, and even no discernible discrimination between age classes at all (Table 2). For example,
Drosophila pseudoobscura females prefer older males and
females mated to older males produce significantly more offspring (a direct benefit that is possibly due to increased investment in sperm or accessory fluids; [26]). The only other study
listed in Table 2 conducted in a species with a potential
resource-based mating system failed to document a preference
for older males [74], although the design of this study did not
differentiate between female choice and male competition.
Nevertheless, the authors conclude that the lack of preference
suggests that direct benefits do not drive age-based mating
preferences in this species [74]. For species where males
provide direct benefits and older males are better parents or
have better resources (e.g. territories, food), then the negative
effects of male age may be masked by the positive effects of
their ability to provide parental care or other resources.
In other words, the direct benefits old males provide might
outweigh the indirect costs of their comparatively poorer
gamete quality [16]. There is a clear need for additional
studies, specifically those assaying female mate preference
in resource-based mating systems where sperm traits can also
be quantified.
Are females making ‘‘good’’ choices?
While the evidence for age-based female mate preference is
clearly mixed, the key question is whether females are making
choices that result in high fertilization success and high offspring fitness? For example, D. pseudoobscura females prefer
older males, but the sons produced from young and old males
do not differ in their mating success [26]. In contrast, preference for young males was exhibited in non-virgin female bulb
mites, with a corresponding fertilization advantage with
younger males [31]. However, a later study found that females
613
Problems & Paradigms
Case study
S. L. Johnson and N. J. Gemmell
Problems & Paradigms
S. L. Johnson and N. J. Gemmell
did not discriminate between young and old males, yet daughters of young males had higher fecundity than daughters of
older males [60]. Finally, female cabbage beetles prefer intermediate aged males and matings with intermediate aged
males result in higher offspring hatching rates [59].
While there is increasing evidence that sperm traits influence fertilization success and offspring fitness, only one
study that we know of has assessed both sperm traits and
female mate preference [24]. Old male guppies tend to produce
slower-swimming sperm than younger males, but females did
not discriminate between young and old males in a mate
choice experiment [24]. This is the largest gap in our knowledge, thus there is a clear need to conduct female mate
preference tests in systems where we can also assess male
sperm traits, fertilization success and offspring fitness.
A potential issue is that preference tests are typically done
by presenting a female with males of varying age (e.g. young
vs. old or young vs. intermediate vs. old; Table 2), but in most
cases it is impossible to separate female choice from male
competitive interactions (but see [24, 75]). Assessing female
preference in the absence of male competition [24, 75], followed by competitive experiments (either in vitro or where
females are presented with two or three males and allowed to
mate) may be a better approach. Further, there are a number of
confounding variables that may be obscuring our ability to
detect female mate preferences and the consequences of these
preferences.
What might we be missing?
Male mating history may confound age-related patterns
A potential issue in studies investigating age-related fertility is
that male mating history is rarely standardized [30]. Duration
of abstinence is a known confounder in humans, yet in the
majority of studies there is no attempt to test for abstinence
duration as a potential confounder [3]. Likewise, in nonhuman studies there is little attempt to standardize for mating
history (but see [30, 74]) or at least to test for it as a potential
confounder. For example, females mating with males who
have older stored sperm may suffer reduced fertility.
Whereas, males that mate often, or experience high rates of
sperm competition, may replenish their sperm frequently and
thus have better fertilization success, regardless of age [30,
43]. Along these lines, polyandrous insect species do tend to
have a higher proportion of live sperm in their sperm stores,
compared to monandrous species [76], suggesting that the
frequency of mating and presumably sperm usage has a
positive effect on maintaining sperm quality. Sperm storage
time negatively affected fertilization success and offspring
fitness in the black-legged kittiwake [67] and the sand lizard
[66]. In contrast, patterns of female fecundity and fertilization
success were unrelated to male mating history or sperm age in
the hide beetle [30]. If a particular age class of males (either
young or old) have lower re-mating rates then they will have
stored sperm for longer than males that are mating more often;
hence it may be difficult to separate pre-meiotic effects from
post-meiotic effects [5]. An added complication is that females
mating with highly successful males may also suffer lower
614
Prospects & Overviews
....
reproductive success because of the effects of sperm depletion
[26]. Further, increased sperm production is expected to result
in an increase in male germline cell divisions [20]; hence males
that mate often, should accumulate deleterious mutations
more rapidly. Additional studies investigating the impact of
mating history on sperm traits, male reproductive success and
female mate preferences are necessary.
Female reproductive success and mate preference may
alter with female age
A major criticism of many studies of decline in male fertility
with age in humans is the lack of standardization of female age
[3], an important predictor of fertility [1, 2]. While non-human
studies have been better at controlling for this confounding
factor, it is important to point out why such a control is
necessary. There is evidence that female age directly affects
female reproductive success. For example, older virgin female
cockroaches laid fewer offspring than young virgin females
[77]. In contrast, male mounting frequency, courtship feeding
and cloacal contacts were positively associated with female
age in the common turn, suggesting a mating advantage for
older females [78]. There is also some indirect evidence to
suggest that female age may influence mating success or
subsequent fertilization success [79]. Further, aging females
may be mating with aging males (i.e. assortative mating),
making it difficult to separate the effects of male aging from
female aging effects [5].
One could argue that female mating preference should
alter across the lifespan of a female [80], particularly with
respect to perceived potential for reproduction [81]. There is
evidence that female age directly affects female mate choice.
For example, in the horseshoe crab, monandrous females tend
to be in good condition (younger), whereas polyandrous
females tend to be of lower condition (older; [82]). Few studies
have investigated the effect of male age on mate preference by
females of varying age [59]. In the common lizard, young and
old females increased their fitness by being polyandrous
whereas middle-aged females tended to mate with males of
intermediate age [80]. In contrast, females of all age classes
preferentially mated with middle-aged males in the cabbage
beetle [59]. Alternatively, female mate preference might vary
depending on the quality of the female, such that females alter
their choosiness or even the direction of mating preferences
depending on their own quality [83]. In the zebra finch, only
high-quality females prefer high-quality males’ songs, while
all low-quality females preferred low-quality males’ song [84].
Similarly, in fallow deer, younger females mate with younger
and lower ranking males while older females mated almost
exclusively with dominant males, and this age-related change
in selectivity is likely associated with female body condition
[85]. Overall, we need more studies investigating how male
and female age, together [79], affect female mate preference.
Measurement of sperm traits are influenced by
assay media
Several recent studies show that sperm quality differs in
female bodily fluids versus water or other physiological assay
media [37, 58, 86]. For instance, sperm motile quality was
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
....
Prospects & Overviews
Reproductive compensation may mask female
age-based preference
It is possible that females may be able to make up for any
reduction in offspring fitness resulting from mating with poor
quality mates, through reproductive compensation (RC) via
female parental care or other forms of female investment [88].
For example, in studies where females are experimentally
constrained to reproduce with males they do not prefer,
females enhance fecundity, which is hypothesized to compensate for lower offspring viability [88]. Females may also be able
to compensate via enhanced maternal care [88]. Only a few
taxa in Table 2 exhibit maternal care [28, 35, 89], but a
comparison of the fertilization success and offspring fitness
resulting from mating with young and old males were not
assayed. Future studies should thus be careful when interpreting data in systems where reproductive compensation might
be possible, though reproductive compensation is predicted to
be rare in nature [81]. Increased investment into offspring
produced with high-quality mates (differential allocation) is
expected to be more common [81]. Still, male age could be an
important mediator of RC. Studies comparing reproductive
success with old and young males in systems where females
are known to exhibit reproductive compensation would be
informative.
Sex ratio may influence male dominance and female mate
preferences
A recent study highlights how the sex ratio in a population
studied may be a further confounding variable in studies
investigating a decline in male fertility [35]. The relationship
between male age and male social status differs depending on
the level of intrasexual competition in domestic fowl: under
intense competition (six males:three females) socially subordinate males were older than males of higher status. However,
under a female biased sex ratio (three males:six females),
common in this species, male social status is not affected
by male age, so that aging males were able to achieve dominant status and monopolized sexual access to females. When
this happens, however, females pay a substantial fertility cost
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
[35]. This finding highlights the need to investigate how
sex ratio affects age-based female mate preference in other
species, particularly those that have complex social mating
dynamics.
Cross-sectional designs prevent examination of how
fertility alters over time
Studies rarely follow individual males throughout their lives,
but instead assign discrete age classes that may potentially
conceal some age-related mating patterns, particularly if the
age classes assigned do not span the life of the organism [36].
A few studies have undertaken longitudinal studies of male
aging but these are also inconclusive [35, 36, 90]. Copulation
propensity and the sperm swimming velocity of individual
males did not decline with age in fowl, but semen transfer
and total number of sperm ejaculated were associated with a
non-significant decline [35]. Whereas, in the hide beetle, fertilization success increased following male emergence but
declined again when males were aged beyond 11 weeks
[36]. Following individual males throughout their lives allows
the examination of trade-offs between early and late life
history components [35], one of the key arguments against
female preference for older males [18]. Further, assessing
whether different males (i.e. haplotypes; see Box 2) age at
different rates might provide clues as to why females might
still mate with older males.
Evolutionary consequences of a decline
in male fertility with age
Older males may be disadvantaged under conditions of
sperm competition
Males often must compete for reproductive opportunities
and if a given male’s sperm function declines with age then
that male may well be less successful under conditions of
sperm competition [62]. Sperm swimming speed has been
shown to positively correlate with competitive fertilization
success in birds [91, 92] and externally fertilizing fishes
[93, 94]. A number of studies also have documented a
decline in male competitive success with increasing age
[31, 35, 79, 95]; but see [96]. However, few studies assay sperm
quality when investigating the effects of male age on sperm
competition. A recent study in fowl found that older males
tend to ejaculate sperm of lower swimming velocity [35]. An
additional experiment in this study demonstrated that in
groups where the dominant male was young, old subordinate
males failed to gain any paternity, but in groups where the
dominant male was old, young subordinate males were able to
obtain some paternity [35]. Other studies observe no discernable effect with age. Sperm competition success did not
correlate with male age in the guppy, even though sperm
swimming speed tends to decline with age [24]. These ambiguous findings indicate that additional studies are needed to
determine whether older males are less reproductively competitive than younger males, how this relates to sperm traits,
and most importantly, whether their offspring have lower
fitness.
615
Problems & Paradigms
found to decline in old male barn swallows, but this decline is
much more pronounced when sperm quality is assayed in
medium from the female oviduct compared to neutral medium
[37]. Similarly, sperm quality is greater when the sperm of
chinook salmon are activated in female ovarian fluid compared to activation in fresh water [86] and a given male’s
sperm quality is dependent on the female’s ovarian fluid in
which it is activated [87]. In the guppy, sperm quality was
significantly lower when measured in a solution containing
ovarian fluid from a sister as compared with that from an
unrelated female [58]. These findings have important implications for studies of sperm quality in humans and other organisms because previous studies exclusively have considered
sperm quality in neutral medium, which may not represent
sperm quality under natural conditions [37, 86]. This is
particularly an issue with regard to studies of sperm competition and may explain some of the ambiguous results found in
studies of age-related decline in fertility [24].
S. L. Johnson and N. J. Gemmell
S. L. Johnson and N. J. Gemmell
Problems & Paradigms
Box 2
Mechanisms responsible for decline in sperm
traits with age
The mechanisms responsible for age-dependent patterns
of decline in sperm fitness are not fully understood.
However, reductions in sperm traits are influenced by both
pre-meiotic aging of somatic and germ cells (driven by
accumulating genetic damage in the male germline), and
post-meiotic aging of the spermatozoa (determined by the
aging of individual germ cells following meiosis; reviewed
in ref. [5]).
Damage by oxidative stress is clearly an important
contributor to both pre-meiotic and post-meiotic aging
[5, 9, 39–41]. Oxidative stress is a result of an imbalance
between reactive oxygen species (ROS) production and
endogenous antioxidant defense [40]. A decline in sperm
traits in males has been correlated with the excessive
generation of ROS by sperm mitochondria and the stimulation of lipid peroxidation [41], with increased levels of
ROS in semen positively correlated with age [42].
Increased ROS are correlated with decreased sperm motility [41] and loss of fertilizing efficiency [43]. Increased ROS
levels are also correlated positively with nuclear DNA fragmentation [9, 39], mtDNA point mutation [44, 45], and
Females may engage in polyandry to reduce the costs of
mating with older males
It has been suggested that polyandry may serve to reduce the
costs imposed to the female by male age [5, 24, 62]. If mating
with old males is costly because their sperm are of lower
genetic quality due to an accumulation of deleterious
mutations in the germ line and these mutations affect sperm
competitiveness by reducing sperm traits [62], then females
will benefit from polyandry, via sperm competition, and may
reduce the risk that eggs will be fertilized by lower quality
sperm (i.e. sperm from old males; [24, 62]). In such a case,
young males are predicted to be favored in sperm competition
over older males [24]. This would be particularly important in
species where it is difficult to determine the relative age of a
potential mate, or to avoid copulations with old males (for
example due to sexual harassment). The evidence is mixed for
this hypothesis [24, 62, 79, 95, 96]; therefore, additional studies are needed in order assess whether polyandry has evolved
in order to avoid mating with older males that might carry
deleterious mutations.
Sometimes female choice is constrained
Reduced fecundity due to a decline in male fertility with age
may ultimately represent a constraint to female mate choice,
particularly if dispersal limitation and intrasexual competitive
interactions limit potential breeding partners. Likewise, male
coercion, arranged marriages, resource acquisition, and predation risk can all constrain mate choice [88]. For example,
flies, pipefishes, and mice sometimes court under predation
616
Prospects & Overviews
....
possibly mtDNA content [46, 47], which are in turn linked
with heightened sperm dysfunction and abnormality [39, 44]
and offspring mortality [48]. In addition, we know that individuals with differing mtDNA haplotypes can differ in their
basal rate of metabolism [49], ROS production [45], and
sperm motility [49], and therefore, potentially sperm aging.
One area of debate in humans is whether the decline in
sperm traits observed in various cross-sectional studies is
attributable to the environmental conditions now experienced by modern humans (e.g. ionizing radiation, toxins,
pollutants) which may contribute to an apparent recent
global decline in human sperm traits [50, 51] or whether
this represents a natural decline in male fertility with
increasing age. A recent study demonstrates that male
reproductive traits have high heritability, suggesting that
genetic factors directly contribute to the age-related
decline in sperm traits [52]. However, it has also been
suggested that epigenetic factors (e.g. DNA methylation,
histone modifications, and non-coding RNAs) might influence aging in the male germline [53]. In support of this
hypothesis, DNA methylation changes accumulate in
sperm with increasing paternal age [54]. Overall, the exact
drivers of the age-dependent relationships reported have
yet to be determined; hence, more research is necessary
to further understand the mechanisms associated with a
decline in male fertility with age.
risk and experience limits to dispersal that constrain their
mate preferences [88]. Females may however be able to
increase reproductive effort and investment in offspring to
make up for any reduction in offspring fitness resulting from
reproductive constraints, through reproductive compensation
[88]. Studies investigating the influence of male age on sperm
traits, reproductive success and female mate preferences of
organisms that are subject to reproduction under various
constraints would be enlightening.
Male aging can lead to conflict between the sexes
Male aging can lead to sexual conflict between the sexes through
direct (male fertility) or indirect (offspring viability) reproductive
costs to a female, [29, 35, 97]. Aging has been shown to affect
sperm traits (Table 1) and in some cases this may select for
females that avoid mating with old males (Table 2). But, evolution will tend to favor old males able to coerce females into
mating with them, generating sexual conflict over mating [29].
Males that are able to monopolize access to females may suffer
from reduced fertilization success or if they are capable of
fertilizing eggs then the resulting offspring may have reduced
fitness [29, 35, 97]. For example, in the mealworm beetle, mating
with old males is particularly costly. Not only do females mated
to old males produce offspring significantly smaller than those
mated with young males, but matings with old males are more
likely to result in failed sperm transfer [29]. Further, mating
reduces female attractiveness, meaning that females will have a
lower probability of gaining additional matings [29]. Likewise,
sexual conflict can lead to female infertility [98] or accelerate
females aging [98]. Finally, in fowl, dominant males monopol-
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
....
Prospects & Overviews
Conclusions
The apparent paradox between age-related declines in male
fertility and female mate choice for older males is likely manifest in many systems, but has not yet been rigorously explored.
Past work has variously investigated: (i) the change in sperm
traits with age ([3]; refs. within Table 1) (ii) the effect of age on
mating success and fertilization success (refs. within Table 2),
(iii) the mechanisms responsible for the change in fertility [9,
47], and (iv) age-dependent mate preferences (refs. within
Table 2). To date, only a few studies have investigated the
effect of mating frequency while also assessing the role of male
age on fecundity and fertilization success [30], but no study
has examined sperm motility, male fertilization success, offspring fitness and female preference, while also measuring the
mechanisms responsible for the change in fertility. In order to
tease age, lifestyle and genetic factors apart, studies measuring factors including, but not limited to, seminal ROS, DNA
fragmentation and nuclear and mtDNA point mutation, and
mtDNA content in a longitudinal study are necessary. This will
provide much needed information on how these measures
alter with age and mating history, and importantly, how
age and mating history might interact, negatively or positively, to affect sperm traits and male fitness. Testing whether
females can distinguish and thus exert preference for males
with superior fertility, whether these preferred males are more
competitive with regard to sperm competition and most importantly whether these preferred males produce offspring of
higher fitness is necessary in order to determine whether mate
choice enables females to effectively eliminate the potential
threat to her fitness, and that of her offspring, due to mating
with males with high levels of sperm damage.
Acknowledgments
We thank two anonymous reviewers for comments that
improved the manuscript. Robbie McPhee assisted with figure
design. Funding support was provided by University of Otago
start-up funds (NJG), Otago School of Medical Sciences Dean’s
Bequest Funds (NJG and SLJ) and a Royal Society of New
Zealand Marsden Fund Fast-Start Grant (SLJ).
References
1. Maheshwari A, Hamilton M, Bhattacharya S. 2008. Effect of female
age on the diagnostic categories of infertility. Hum Reprod 23: 538.
2. Belloc S, Cohen-Bacrie P, Benkhalifa M, Cohen-Bacrie M, et al. 2008.
Effect of maternal and paternal age on pregnancy and miscarriage rates
after intrauterine insemination. Reprod Biomed Online 17: 392–7.
3. Kidd SA, Eskenazi B, Wyrobek AJ. 2001. Effects of male age on semen
quality and fertility: a review of the literature. Fertil Steril 75: 237–48.
4. Kühnert B, Nieschlag E. 2004. Reproductive functions of the ageing
male. Hum Reprod Update 10: 327–39.
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
5. Pizzari T, Dean R, Pacey A, Moore H, et al. 2008. The evolutionary ecology
of pre- and post-meiotic sperm senescence. Trends Ecol Evol 23: 131–40.
6. Sartorius GA, Nieschlag E. 2010. Paternal age and reproduction. Hum
Reprod Update 16: 65–79.
7. Sloter E, Schmid TE, Marchetti F, Eskenazi B, et al. 2006. Quantitative
effects of male age on sperm motion. Hum Reprod 21: 2868–75.
8. Rybar R, Kopecka V, Prinosilova P, Markova P, et al. 2011. Male
obesity and age in relationship to semen parameters and sperm chromatin integrity. Andrologia 43: 286–91.
9. Aitken RJ, De Iuliis GN, McLachlan RI. 2009. Biological and clinical
significance of DNA damage in the male germ line. Int J Androl 32: 46–56.
10. Brooks R, Kemp DJ. 2001. Can older males deliver the good genes?
Trends Ecol Evol 16: 308–13.
11. Kokko H, Lindstrom J. 1996. Evolution of female preference for old
mates. Proc Roy Soc Lond B Biol 263: 1533–8.
12. Proulx SR, Day T, Rowe L. 2002. Older males signal more reliably. Proc
Roy Soc Lond B Biol 269: 2291–9.
13. Buss DM. 1989. Sex differences in human mate preferences: evolutionary hypotheses tested in 37 cultures. Behav Brain Sci 12: 1–49.
14. Fieder M, Huber S. 2007. Parental age difference and offspring count in
humans. Biol Lett 3: 689–91.
15. Andersson M. 1994. Sexual Selection. Princeton, New Jersey:
Princeton University Press.
16. Beck CW, Promislow DEL. 2007. Evolution of female preference for
younger males. PLoS One 2: e939.
17. Manning JT. 1985. Choosy females and correlates of male age. J Theor
Biol 116: 349–54.
18. Hansen TF, Price DK. 1995. Good genes and old age: do old mates
provide superior genes? J Evol Biol 8: 759–78.
19. Hansen T, Price D. 1999. Age- and sex-distribution of the mutation load.
Genetica 106: 251–62.
20. Ellegren H. 2007. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc Roy Soc B-Biol Sci 274: 1.
21. Beck CW, Powell LA. 2000. Evolution of female mate choice based on
male age: are older males better mates? Evol Ecol Res 2: 107–18.
22. Syntin P, Robaire B. 2001. Sperm structural and motility changes during
aging in the Brown Norway rat. J Androl 22: 235–44.
23. Thongtip N, Saikhun J, Mahasawangkul S, Kornkaewrat K, et al.
2008. Potential factors affecting semen quality in the Asian elephant
(Elephas maximus). Reprod Biol Endocrinol 6: 9.
24. Gasparini C, Marino IAM, Boschetto C, Pilastro A. 2010. Effect of
male age on sperm traits and sperm competition success in the guppy
(Poecilia reticulata). J Evol Biol 23: 124–35.
25. Kanuga MK, Benner MJ, Doble JA, Wilson-Leedy JG, et al. 2011.
Effect of aging on male reproduction in zebrafish (Danio rerio). J Exp Zool
Part A 315A: 156–61.
26. Avent TD, Price TAR, Wedell N. 2008. Age-based female preference in
the fruit fly Drosophila pseudoobscura. Anim Behav 75: 1413–21.
27. Somashekar K, Krishna MS. 2011. Evidence of female preference for
older males in Drosophila bipectinata. Zool Stud 50: 1–15.
28. De Luca P, Cocroft R. 2008. The effects of age and relatedness on
mating patterns in thornbug treehoppers: inbreeding avoidance or
inbreeding tolerance? Behav Ecol Sociobiol 62: 1869–75.
29. Carazo P, Molina-Vila P, Font E. 2011. Male reproductive senescence
as a potential source of sexual conflict in a beetle. Behav Ecol 22: 192–8.
30. Jones TM, Elgar MA. 2004. The role of male age, sperm age and mating
history on fecundity and fertilization success in the hide beetle. Proc Roy
Soc Lond B Biol 271: 1311–8.
31. Radwan J, Michalczyk L, Prokop Z. 2005. Age dependence of male
mating ability and sperm competition success in the bulb mite. Anim
Behav 69: 1101–5.
32. Eskenazi B, Wyrobek AJ, Sloter E, Kidd SA, et al. 2003. The association of age and semen quality in healthy men. Hum Reprod 18: 447–54.
33. Wyrobek AJ, Eskenazi B, Young S, Arnheim N, et al. 2006. Advancing
age has differential effects on DNA damage, chromatin integrity, gene
mutations, and aneuploidies in sperm. Proc Nat Acad Sci USA 103:
9601–6.
34. Rijsselaere T, Maes D, Hoflack G, de Kruif A, et al. 2007. Effect of body
weight, age and breeding history on canine sperm quality parameters
measured by the Hamilton-Thorne analyser. Reprod Domest Anim 42:
143–8.
35. Dean R, Cornwallis CK, Lovlie H, Worley K, et al. 2010. Male reproductive senescence causes potential for sexual conflict over mating.
Curr Biol 20: 1192–6.
36. Hale JM, Elgar MA, Jones TM. 2008. Sperm quantity explains agerelated variation in fertilization success in the hide beetle. Ethology 114:
797–807.
617
Problems & Paradigms
ize access to females in a group, but if the dominant male is an
old male then females suffer from reduced fertilization success,
presumably because the old males are not able to fertilize all of
the available eggs, creating conflict over mating [99]. With such
a high cost to female reproductive success, it is puzzling that
females do not eject the sperm from old males [99].
S. L. Johnson and N. J. Gemmell
Problems & Paradigms
S. L. Johnson and N. J. Gemmell
37. Möller AP, Mousseau TA, Rudolfsen G, Balbontin J, et al. 2009.
Senescent sperm performance in old male birds. J Evol Biol 22:
334–44.
38. Wedell N, Ritchie MG. 2004. Male age, mating status and nuptial gift
quality in a bushcricket. Anim Behav 67: 1059–65.
39. Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, et al. 2010. Analysis of
the relationships between oxidative stress, DNA damage and sperm
vitality in a patient population: development of diagnostic criteria. Hum
Reprod 25: 2415–26.
40. Agarwal A, Makker K, Sharma R. 2008. Clinical relevance of oxidative
stress in male factor infertility: an update. Am J Reprod Immunol 59:
2–11.
41. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, et al. 2008.
Significance of mitochondrial reactive oxygen species in the generation
of oxidative stress in spermatozoa. J Clin Endocrinol Metab 93: 3199–
207.
42. Cocuzza M, Athayde KS, Agarwal A, Sharma R, et al. 2008. Agerelated increase of reactive oxygen species in neat semen in healthy
fertile men. Urology 71: 490–4.
43. Siva-Jothy MT. 2000. The young sperm gambit. Ecol Lett 3: 172–4.
44. Spiropoulos J, Turnbull DM, Chinnery PF. 2002. Can mitochondrial
DNA mutations cause sperm dysfunction? Mol Human Reprod 8:
719–21.
45. Moreno-Loshuertos R, Acin-Perez R, Fernandez-Silva P, Movilla N,
et al. 2006. Differences in reactive oxygen species production explain
the phenotypes associated with common mouse mitochondrial DNA
variants. Nat Genet 38: 1261–8.
46. Song GJ, Lewis V. 2008. Mitochondrial DNA integrity and copy number
in sperm from infertile men. Fertil Steril 90: 2238–44.
47. May-Panloup P, Chretien MF, Savagner F, Vasseur C, et al. 2003.
Increased sperm mitochondrial DNA content in male infertility. Hum
Reprod 18: 550–6.
48. Ruiz-Lopez MJ, Espeso G, Evenson DP, Roldan ERS, et al. 2010.
Paternal levels of DNA damage in spermatozoa and maternal parity
influence offspring mortality in an endangered ungulate. Proc Roy
Soc B-Biol Sci 277: 2541–6.
49. Ruiz-Pesini E, Lapeña A-C, Dı́ez-Sánchez C, Pérez-Martos A, et al.
2000. Human mtDNA haplogroups associated with high or reduced
spermatozoa motility. Am J Hum Genet 67: 682–96.
50. Bonde JP. 2010. Male reproductive organs are at risk from environmental hazards. Asian J Androl 12: 152–6.
51. Aitken RJ, Koopman P, Lewis SEM. 2004. Seeds of concern. Nature
432: 48–52.
52. Kosova G, Abney M, Ober C. 2010. Heritability of reproductive fitness
traits in a human population. Proc Natl Acad Sci USA 107: 1772–8.
53. Curley JP, Mashoodh R, Champagne FA. 2011. Epigenetics and the
origins of paternal effects. Horm Behav 59: 306–14.
54. Oakes CC, Smiraglia DJ, Plass C, Trasler JM, et al. 2003. Aging results
in hypermethylation of ribosomal DNA in sperm and liver of male rats.
Proc Nat Acad Sci USA 100: 1775–80.
55. Garcı́a-Palomares S, Pertusa JF, Miñarro J, Garcı́a-Pérez MA, et al.
2009. Long-term effects of delayed fatherhood in mice on postnatal
development and behavioral traits of offspring. Biol Reprod 80: 337–42.
56. Garcı́a-Palomares S, Navarro S, Pertusa JF, Hermenegildo C, et al.
2009. Delayed fatherhood in mice decreases reproductive fitness and
longevity of offspring. Biol Reprod 80: 343–9.
57. Simon L, Lewis SEM. 2011. Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro? Syst Biol
Reprod Med 57: 133–8.
58. Gasparini C, Pilastro A. 2011. Cryptic female preference for genetically
unrelated males is mediated by ovarian fluid in the guppy. Proc Roy Soc
B-Biol Sci 278: 2495–501.
59. Liu XP, Xu J, He HM, Kuang XJ, et al. 2011. Male age affects female
mate preference and reproductive performance in the cabbage beetle,
Colaphellus bowringi. J Insect Behav 24: 83–93.
60. Prokop ZM, Stuglik M, Zabinska I, Radwan J. 2007. Male age, mating
probability, and progeny fitness in the bulb mite. Behav Ecol 18: 597–
601.
61. Pervez A. 2004. The influence of age on reproductive performance of the
predatory ladybird beetle, Propylea dissecta. J Insect Sci 4: 22.
62. Radwan J. 2003. Male age, germline mutations and the benefits of
polyandry. Ecol Lett 6: 581–6.
63. Crow JF. 2000. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 1: 40–7.
64. Torres R, Drummond H, Velando A. 2011. Parentalage and lifespan
influence offspring recruitment: a long-term study in a seabird. PLoS One
6: e27245.
618
Prospects & Overviews
....
65. Velando A, Noguera JC, Drummond H, Torres R. 2011. Senescent
males carry premutagenic lesions in sperm. J Evol Biol 24: 693–7.
66. Olsson M, Schwartz T, Uller T, Healey M. 2007. Sons are made
from old stores: sperm storage effects on sex ratio in a lizard. Biol
Lett 3: 491–3.
67. White J, Wagner RH, Helfenstein F, Hatch SA, et al. 2008. Multiple
deleterious effects of experimentally aged sperm in a monogamous bird.
Proc Natl Acad Sci USA 105: 13947–52.
68. Velando A, Torres R, Alonso Alvarez C. 2008. Avoiding bad genes:
oxidatively damaged DNA in germ line and mate choice. BioEssays 30:
1212–9.
69. Torres R, Velando A. 2003. A dynamic trait affects continuous pair
assessment in the blue-footed booby, Sula nebouxii. Behav Ecol
Sociobiol 55: 65–72.
70. Velando A, Drummond H, Torres R. 2006. Senescent birds redouble
reproductive effort when ill: confirmation of the terminal investment
hypothesis. Proc Roy Soc B-Biol Sci 273: 1443–8.
71. Torres R, Velando A. 2007. Male reproductive senescence: the price of
immune-induced oxidative damage on sexual attractiveness in the bluefooted booby. J Anim Ecol 76: 1161–8.
72. Velando A, Drummond H, Torres R. 2010. Senescing sexual ornaments recover after a sabbatical. Biol Lett 6: 194–6.
73. Kokko H. 1998. Good genes, old age and life-history trade-offs. Evol
Ecol 12: 739–50.
74. Milonas PG, Andow DA. 2010. Virgin male age and mating success
in Ostrinia nubilalis (Lepidoptera: Crambidae). Anim Behav 79: 509–14.
75. Verburgt L, Ferreira M, Ferguson JWH. 2011. Male field cricket
song reflects age, allowing females to prefer young males. Anim
Behav 81: 19–29.
76. Hunter FM, Birkhead TR. 2002. Sperm viability and sperm competition
in insects. Curr Biol 12: 121–3.
77. Moore PJ, Moore AJ. 2001. Reproductive aging and mating: the ticking
of the biological clock in female cockroaches. Proc Nat Acad Sci USA
98: 9171.
78. Gonzalez-Solis J, Becker PH. 2002. Mounting frequency and number
of cloacal contacts increase with age in common terns Sterna hirundo.
J Avian Biol 33: 306–10.
79. Jones TM, Featherston R, Paris D, Elgar MA. 2007. Age-related sperm
transfer and sperm competitive ability in the male hide beetle. Behav
Ecol 18: 251–8.
80. Richard M, Lecomte J, De Fraipont M, Clobert J. 2005. Age-specific
mating strategies and reproductive senescence. Mol Ecol 14: 3147–55.
81. Harris WE, Uller T. 2009. Reproductive investment when mate quality
varies: differential allocation versus reproductive compensation. Philos
Trans Roy Soc B 364: 1039–48.
82. Johnson SL, Brockmann HJ. 2012. Alternative reproductive tactics in
female horseshoe crabs. Behav Ecol, in press, DOI: 10.1093/beheco/
ars063.
83. Härdling R, Kokko H. 2005. The evolution of prudent choice. Evol Ecol
Res 7: 697–715.
84. Holveck M-J, Riebel K. 2010. Low-quality females prefer low-quality
males when choosing a mate. Proc Roy Doc Lond B Biol 277: 153–60.
85. Farrell ME, Briefer E, McElligott AG. 2011. Assortative mating in
fallow deer reduces the strength of sexual selection. PLoS One 6: e18533.
86. Rosengrave P, Montgomerie R, Metcalf VJ, McBride K, et al. 2009.
Sperm traits in chinook salmon depend upon activation medium:
implications for studies of sperm competition in fishes. Can J Zoo 87:
920–7.
87. Rosengrave P, Gemmell NJ, Metcalf V, McBride K, et al. 2008.
A mechanism for cryptic female choice in chinook salmon. Behav
Ecol 19: 1179–85.
88. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, et al. 2007. The
hypothesis of reproductive compensation and its assumptions about
mate preferences and offspring viability. Proc Nat Acad Sci USA 104:
15023–7.
89. Alonso JC, Magana M, Palacin C, Martin CA. 2010. Correlates of male
mating success in great bustard leks: the effects of age, weight, and
display effort. Behav Ecol Sociobiol 64: 1589–600.
90. Hoikkala A, Saarikettu M, Kotiaho JS, Liimatainen JO. 2008. Agerelated decrease in male reproductive success and song quality in
Drosophila montana. Behav Ecol 19: 94–9.
91. Birkhead T, Martinez J, Burke T, Froman D. 1999. Sperm mobility
determines the outcome of sperm competition in the domestic fowl. Proc
Roy Soc Lond B Biol 266: 1759–64.
92. Denk AG, Holzmann A, Peters A, Vermeirssen ELM, et al. 2005.
Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16: 825.
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
....
Prospects & Overviews
Bioessays 34: 609–619,ß 2012 WILEY Periodicals, Inc.
101.
102.
103.
104.
105.
106.
107.
108.
miscuous passerine, the tree swallow Tachycineta bicolor. Behav Ecol
Sociobiol 64: 1473–83.
Garcia-Gonzalez F, Simmons LW. 2005. Sperm viability matters in
insect sperm competition. Curr Biol 15: 271–5.
Casselman S, Montgomerie R. 2004. Sperm traits in relation to male
quality in colonial spawning bluegill. J Fish Biol 64: 1700–11.
Gañán N, Sestelo A, Garde JJ, Martı́nez F, et al. 2010. Reproductive
traits in captive and free-ranging males of the critically endangered
Iberian lynx (Lynx pardinus). Reproduction 139: 275–85.
Pukazhenthi BS, Togna GD, Padilla L, Smith D, et al. 2011. Ejaculate
traits and sperm cryopreservation in the endangered Baird’s tapir
(Tapirus bairdii). J Androl 32: 260.
Fricke C, Maklakov AA. 2007. Male age does not affect female fitness
in a polyandrous beetle, Callosobruchus maculatus. Anim Behav 74:
541–8.
Krishna MS, Santhosh HT, Hegde SN. 2012. Offspring of older males
are superior in Drosophila bipectinata. Zool Stud 51: 72–84.
Burns JG, Mery F. 2010. Transgenerational memory effect of ageing in
Drosophila. J Evol Biol 23: 678–86.
Linder J, Rice W. 2005. Natural selection and genetic variation for
female resistance to harm from males. J Evol Biol 18: 568–75.
619
Problems & Paradigms
93. Gage MJG, Macfarlane CP, Yeates S, Ward RG, et al. 2004.
Spermatozoal traits and sperm competition in Atlantic salmon: relative
sperm velocity is the primary determinant of fertilization success. Curr
Biol 14: 44–7.
94. Gasparini C, Simmons LW, Beveridge M, Evans JP. 2010. Sperm
swimming velocity predicts competitive fertilization success in the green
swordtail Xiphophorus helleri. PLoS One 5: e12146.
95. Schäfer MA, Uhl G. 2002. Determinants of paternity success in the
spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and
female mating behaviour. Behav Ecol Sociobiol 51: 368–77.
96. Hoysak J, Liley NR, Eric BT. 2004. Raffles, roles, and the outcome of
sperm competition in sockeye salmon. Can J Zoo 82: 1017–26.
97. Dean R, Bonsall MB, Pizzari T. 2007. Aging and sexual conflict.
Science 316: 383–4.
98. Bonduriansky R, Maklakov A, Zajitschek F, Brooks R. 2008. Sexual
selection, sexual conflict and the evolution of ageing and life span. Funct
Ecol 22: 443–53.
99. Dean R, Nakagawa S, Pizzari T. 2011. The risk and intensity of sperm
ejection in female birds. Am Nat 178: 343–54.
100. Kleven O, Fossoy F, Robertson RJ, Rudolfsen G. 2010. Sperm
quantity and quality effects on fertilization success in a highly pro-
S. L. Johnson and N. J. Gemmell