(2021) 21:164
Kamimura et al. BMC Ecol Evo
https://doi.org/10.1186/s12862-021-01901-x
BMC Ecology and Evolution
Open Access
RESEARCH
Evolution of nuptial gifts and its
coevolutionary dynamics with male-like
persistence traits of females for multiple mating
Yoshitaka Kamimura1*, Kazunori Yoshizawa2, Charles Lienhard3, Rodrigo L. Ferreira4 and Jun Abe5
Abstract
Background: Many male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed
remating of the females, resulting in higher paternity. Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and selection on females to increase their mating
rate, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to
simulate such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating
(female trait). Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition.
We also analyzed the causes and consequences of this type of traits, taking double receptacles for nutritious seminal
gifts, which are known to occur in an insect group with a “female penis” (Neotrogla spp.), as an illustrative example.
Results: Our individual-based simulations demonstrated that female-female competition for male-derived nutrients
always occur when the environment is oligotrophic and mating costs are low for females. However, a positive correlation between donated gift size and the resultant paternity gain was a requisite for the co-occurrence of large gifts and
females’ competitive multiple mating for the gifts. When gift donation satisfied female demands and thus resulted in
monandry, exaggeration of nuptial gift size also occurred under the assumption that the last male monopolizes paternity. The evolution of double slots for gift acquisition and digestion (female persistence trait) always occurred when
males could not satisfy the demands of females for gifts. However, through coevolutionary reduction in male gift size,
fixation of this trait in a population drastically reduced the average female fitness.
Conclusion: Sperm usage patterns, which have rarely been examined for animals with nuptial gifts, can be a critical
factor for determining the extent of exaggeration in nuptial gifting. Sex-role reversals in mate competition, as a result
of donation of nuptial gifts from males to females, can involve the evolution of male-like, persistent traits in females
that reduce population productivity, as is the case with persistence traits in males.
Keywords: Nuptial gift, Paternity determination mechanism, Coevolution, Female persistence trait, Female penis, Sex
role reversal
*Correspondence: kamimura@fbc.keio.ac.jp
1
Department of Biology, Keio University, Yokohama 223-8521, Japan
Full list of author information is available at the end of the article
Background
Nuptial gifts, any non-gametic materials transferred from
one sex (usually male) to another during courtship and
mating that improve donor fitness, are widely observed
in many groups of animals, such as insects, arachnids,
molluscs, amphibians, birds, and mammals including
humans [1, 2]. In some cases, male-derived “gifts” can be
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Kamimura et al. BMC Ecol Evo
(2021) 21:164
detrimental to female recipients, as with the love darts
of land snails and anti-aphrodisiac seminal peptides of
Drosophila fruit flies, both of which mitigate the intensity of sperm competition in female sperm storage organs
[3, 4]. However, in many cases, males supply and benefit
females with nutritious materials such as prey items they
have collected or voluminous secretions from male internal/external glands [1, 5].
Although this phenomenon is widely observed in the
animal kingdom, there is continuing debate on its primary function [6–13]. Since females of some animals
accept mating (and sperm transfer) only while consuming
a gift, males may donate the gift to obtain mating opportunities (i.e., mating effort hypothesis). In addition to
nourishing female recipients, nutrition from nuptial gifts
can be passed to offspring sired by the male donor, and
thus can function as paternal investment (i.e., paternal
investment hypothesis: [9, 11, 13]). Recent studies suggest that these two hypotheses are not mutually exclusive
and are difficult to discriminate, because male-derived
nutrients cannot be properly allocated to the offspring of
respective donors without a positive correlation between
the extent of mating effort by males and their paternity
success [1].
Regardless of the ultimate benefits for males, a large
nutritious gift is costly for the male to obtain or produce (reviewed in [5]), although it may be more attractive to females or may enable transfer of more sperm
[1, 14, 15]. Accordingly, donation of exaggerated nuptial
gifts may cause partial reversals in sex roles under certain circumstances like limited food. Thus, in contrast
to conventional animals where males more actively seek
mating opportunities, females compete for multiple mating opportunities to obtain more nuptial gifts in animals with sex-reversed mate competition [13, 16–18].
Increased polyandry can result in more severe sperm
competition, changing the cost–benefit balance for males
of preparing nuptial gifts. Although several models have
been proposed to date for elucidating the evolution of
nuptial gifts [10, 19, 20], they did not encompass these
possible coevolutionary feedbacks between the sexes for
the trading of gifts. The patterns of female sperm storage
and use, which determine the benefits in paternity gain of
donating a given size of gift, are possible pivotal factors
for shaping the coevolutionary dynamics in the trading of
nuptial gifts. However, no theoretical studies have explicitly incorporated these aspects so far.
To analyze the coevolutionary process between malederived gifts and female propensity for multiple matings
for the first time, we develop an individual-based model
in this study incorporating post-copulatory sexual selection. The effects of the environmental/ecological factors
(mating costs for females and resource availability) and
Page 2 of 14
sperm usage patterns on the coevolutionary process are
also evaluated. Since male donors cannot exactly control
the size of prey items, we model the evolution of seminal
gift size, which can be treated as an evolvable trait (e.g.,
[21]).
Evolution of female morphology for gift‑acquisition
Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition. As an
example of this type of traits, the members of Neotrogla
(Insecta: Psocodea: Prinoglarididae: Sensitibillini) are of
special interest. In all four known species of this genus,
females possess an evolutionarily novel penis-like structure, termed a gynosome [22]. During copulation which
lasts for a long period (41–73 h in N. curvata) with the
female positioned above the male, a female inserts this
“female penis” to the vagina-like male genitalia [22]. During this, seminal fluid which contains voluminous and
potentially nutritious seminal substances is transferred to
the female through the gynosome and an elongated duct
(spermathecal duct) [22]. Then, a voluminous ejaculate
forms a gigantic, bottle-shaped capsule (spermatophore)
in the female body [22, 23]. The gynosome is ornamented with species-specific lobes and/or spine bundles,
which are accommodated in specialized pouches of the
male genital cavity during copulation [22]. Since they
live in dry, nutritionally poor caves in Brazil, the gynosome likely represents a female adaptation for unwilling
male mates to better grasp them and to exploit seminal
gifts, though no physical damage has been detected in
male “vagina”, [22, 24]. Although female-female competition for seminal gifts has not been directly observed for
Neotrogla spp., females of a related species with similar
spermatophores (Psocodea: Trogiidae: Lepinotus) compete for access to males [25–27].
Moreover, females of Neotrogla and those of related
genera of the tribe Sensitibillini (Afrotrogla and Sensitibilla) have also developed a specialized structure, termed
a spermathecal plate, in their sperm storage organ (spermatheca). In Neotrogla (and possibly also in Afrotrogla and Sensitibilla), this evolutionarily novel organ is
equipped with twin slots that enable retention and digestion of two seminal gifts simultaneously [22–24, 28]. By
contrast, females of related groups with only a single
slot for nuptial gift can accept another mating only after
digestion of the content of a spermatophore received at
the preceding mating (for example, in Lepinotus [26]).
Given that Neotrogla females mate multiply as evidenced
by up to two full and nine emptied spermatophore capsules in their spermatheca [22], the spermathecal plate
of this genus can be considered another female persistence trait for competitively obtaining male-derived gifts
in rapid succession. As an extension of our basic model,
Kamimura et al. BMC Ecol Evo
(2021) 21:164
we also analyzed the causes and consequences of the evolution of this female persistence trait, i.e., twin slots for
gift reception and digestion, in coevolutionary dynamics
between male gift size and female propensity for multiple
mating.
Outline of the simulation methods
We simulated the coevolutionary dynamics between two
traits with sex-specific expression in a population of sexually-reproducing, diploid organisms of a constant size
(500 females plus 500 males): the size (volume) of nutritive seminal gifts produced by males (V) and female propensity for multiple mating to obtain gifts (the number of
additional matings: M). Each of these traits were assumed
to be determined by alleles on a single locus (v1 and v2,
and m1 and m2), which were continuously variable and
subject to recurrent mutations. No linkage was assumed
between these two loci. We made only two basic assumptions on the effects of these traits on male and female fitness: (1) the offspring number of a female (fecundity) is a
saturation function (Fig. 1) of the cumulative volume of
seminal gifts (r) received in all of her previous matings,
reduced by mating costs (c) multiplied by the number of
realized matings (MR), and (2) reception of a gift, which
occupies a slot for its digestion, delays subsequent matings of the female, in a manner proportional to the gift
size. Thus, given that males acquire a limited amount
Fig. 1 Female fecundity as a saturating function of cumulative
seminal nutrients from males (r), based on the assumption that a
given volume of nuptial gift will increase the female’s fitness more
effectively when the female is starving. When males provide a
seminal gift of size 500 (V = 500), females that mated once should
seek another mating opportunity when the cost of mating is low
(orange arrows, c = 100 per mating), but not under a higher cost (red
arrows, c = 200). See Eqs. (1) and (2) in the main text for the details
Page 3 of 14
of resources for gift production (R), males that produce
large-sized gifts can reduce the probability of remating
of the female mates while increasing their fecundity, but
suffer a reduced number of possible matings (N ≈ R/V;
a size-number trade-off ). To avoid unnecessary complexities, any precopulatory behaviors, such as male-male
combat over mates or female choice on gift size or males,
were not incorporated.
Since sperm storage/use patterns of multiply-mated
females are largely unknown for animals with donation
of nuptial gifts [1], we examined four different regimes
for the relationship between the nuptial gift size and
the resultant paternity gain in this study: fair raffle (FR),
equal shares (ES), complete last male (LM), and complete first male (FM) (Fig. 2, Table 1). Simulations were
repeated for each of these four paternity-determination
schemes, in combination with variable resource availability to males (R) and mating costs for females (c).
Results
Coevolution of nuptial gift size and female multiple mating
under different paternity‑determination regimes
Our simulations revealed notable effects of the pattern
of paternity determination on the evolution of gigantic
seminal gifts and female propensity for multiple mating.
Under a given set of parameters, the male seminal gift
size and female propensity for multiple mating rapidly
converged to an equilibrium, usually before the 300th
generation (the left half of Fig. 3a, b; Additional file 1).
Only when females used sperm from each male mate for
fertilization of eggs proportionally to the nuptial gift size
donated (the FR regime) did males evolve a large-sized
gift compared with their lifetime resource budget under
a wide range of parameter sets (male resource budget [R]
and cost of mating for females [c]: Fig. 4A).
Under the situations assumed in our simulation, dividing the limited resource (R) into small-sized gifts could
increase the mating opportunities of males, while a
large-sized nuptial gift could afford males two types of
paternity benefits, namely: (1) siring more offspring than
males who gave a smaller gift to the same mate; and (2)
eliminating the probability of remating by the female as
a post-copulatory guard against remating. Because the
former type of benefit (siring more offspring) occurs only
under the assumption of the FR regime, this can explain
the observed prevalence of the “fewer large” strategy over
“many small” in this regime. Accordingly, females evolve
the propensity to mate multiply for these attractive,
large-sized gifts when available, but males generally cannot satisfy the inflated females’ demands (Figs. 4A, 5A).
Exceptions are when the mating cost is extremely large
(high c) and the environment is eutrophic (high R, the
upper-right corners of Figs. 4A, 5A). Large mating costs
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Fig. 2 A scheme of four different regimes of the relationships between seminal gift size and the resultant paternity. Note that Neotrogla spp. shows
a female-above mating posture similar to many other species of Psocodea
for females reduces the attractiveness of a given size of
gifts, making a few matings optimal for females. The latter condition can shift male strategies to “many small” for
seeking many (virgin) females, rendering their gifts more
unattractive to females.
When the paternity was equally assigned to all mates of
a female (ES) or was monopolized by the first male (FM),
the coevolutionary patterns were quite similar indicating
almost identical sexual selection pressures under these
two regimes. Males generally did not evolve a large-sized
nuptial gift (Fig. 4B, D). As discussed above, this can be
attributed to the lack of paternity benefits proportional
to the donated gift size in these regimes. To collect these
small gifts from many males, females mated more frequently than under the FR regime, especially when mating cost was low and the habitat was eutrophic (Fig. 4B,
D). By increasing the acceptable number of matings,
females usually achieved their optimal number of matings (Fig. 5B, D). An exception is the condition with very
small mating costs and oligotrophic environments (the
lower-left corners of Fig. 4B, D), where additional mating
is always beneficial even for small-sized gifts.
When the last male monopolized the paternity (LM),
males generally evolved larger-sized gifts compared to
the FM (complete first male) and ES (equal shares) paternity-determination regimes (Fig. 4C). To be the last mate,
we can envisage two different strategies: preparing many
small gifts increases the opportunities for being the last
mate by chance (as in the FM and ES regimes), while
provision of a large-sized gift is advantageous because
it reduces the probability of remating by the female. The
latter strategy must be especially effective when females
tend to seek additional mating opportunities because of
low mating cost. Thus, the observed large gifts when c is
low (the lower areas of Fig. 4C) can be a countermeasure
of males for preventing frequent remating of their mates.
When mating is more costly for females, it is less necessary for males to prepare large gifts, and the small-sized
gifts reinforce the females’ reluctancy for further mating. Accordingly, for high c values, females satisfied their
mating demands when the habitat was eutrophic (high R,
Fig. 5C). An important exception is the extremely oligotrophic environments (R = 400) with extremely high cost
of mating (c = 85–95) (the upper-left corners of Figs. 4,
5). Under this combination of parameters, males also
evolve comparatively larger gifts under the ES and FM
regimes, even though it does not result in overly high
mating demands of females that males cannot satisfy.
Given extremely high mating costs for females, males
experience a low risk of sperm competition. In addition,
if males have extremely limited resources for preparing
gifts, premating male-male competition should be also
less severe. Accordingly, males likely shift toward providing the monandrous female as much as their resource
budget allows.
In our simulation, the genetic correlation between seminal gift size ([v1 + v2]/2) and female mating propensity
([m1 + m2]/2), calculated for a pooled population of male
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Table 1 Summary of notations and abbreviations used in this study
Symbol
Definition and designated values
Model parameters
v1, v2
Genotypic values of male seminal gift size from male and female parents, respectively. Initial values were given as a normal distribution (mean ± SD = 20 ± 40) with truncation (≥ 20)
V
Phenotypic value of male seminal gift size, calculated as (v1 + v2)/2
Vlast
Seminal volume of the last mating of a focal male (Eq. 5)
m1, m2
Genotypic values of female acceptable number of matings from male and female parents, respectively. Initial values were given as
a normal distribution (mean ± SD = 0.5 ± 2) with truncation (≥ 0)
M
Phenotypic value of female acceptable number of additional matings (= propensity for multiple mating), calculated as
(m1 + m2)/2
MR
Realized number of matings by females
MO
Optimal number of matings by females, given by solving Eq. 2 with the mean V
2s
Dominant gene for producing twin slots for receiving gifts
1s
Recessive gene for producing a single slot for receiving gifts
2S
Females of the genotype 2s/2s or 2s/1s, having twin slots for receiving gifts
1S
Females of the genotype 1s/1s, having a single slot for receiving gifts
R
Mean total volume of resource for producing seminal gifts, ranged from 400 (oligotrophic) to 1300 (eutrophic) by an increment of
100. Each male has a resource budget extracted from a truncated normal distribution mean ± SD = R ± 0.2R (> 0)
N
Possible number of matings for a focal male, given as R/V, rounded up to the nearest integer
n
Realized number of matings for a focal male
r
Cumulative volume of gifts received by a female
b
Fertilization efficiency (Eq. 1; Fig. 1), given as a constant (b = 0.002)
c
Female mating cost (per mating), ranged from 5 to 95 by an increment of 10 (Eq. 2)
FF_max
Maximum female reproductive output (Eq. 1), given as a constant (FF_max = 800)
FF_pot(r)
Maximum fecundity of a female, as a function of b, FF_max and r, before reduction by mating costs (Eq. 1)
FF(r, c, MR)
Realized fecundity (= expected fitness) of a female, as a function of b, FF_max, r, MR, and c (Eq. 2)
P
Paternity share of a male in the offspring of a female mate
FM(V)
Expected fitness of a male defined by Eq. 3
Paternity determination regimes
FR
Paternity is determined by fair raffle with respect to the relative gift size received by a focal female
ES
Paternity is equally shared by all male mates
LM
The last male monopolizes paternity
FM
The first male monopolizes paternity
Simulation modes
CON
Control simulation runs with neither invasion of 2S females nor doubling of female number
DS
One 2S female per generation was introduced from the1000th generation and beyond
DF
Number of females were doubled at the 1000th generation and beyond (i.e., 1000 females for 500 males)
and female individuals, was negligibly low (near zero),
and thus elimination of genetic covariance by shuffling
paternal identity did not change the results (Additional
file 2).
The evolution of twin‑slots and its effects
on the coevolutionary processes
We also tested the evolvability and stability of another
female trait, that is, the twin-slot state (2S) for receiving
and digesting two seminal gifts simultaneously, as well as
its effects on the evolution of the other two traits (male V
and female M). For simplicity, we assumed that this trait
is controlled by a single locus, which is independent of
the v and m loci, with two alleles: 2s, a gene for the twinslot state, and 1s, a gene for the single-slot state, where
the former was assumed to be dominant over the latter.
The populations were initiated with single-slot females
(1S, 1s/1s homozygotes). Then, 2s genes were allowed
to invade populations at the mid (the 1000th generation) of 2000-generation simulation runs and beyond
(one spontaneous mutation in each generation), together
with recurrent invasion of single-slot mutants (a female
individual of 1s/1s homozygote per generation) to check
the evolutionary stability of the twin-slot state (2S). Abe
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Fig. 3 a An example of the coevolutionary dynamics observed between the male seminal gift size (V, blue) and the optimal number of matings for
females (MO, red), together with changes in the realized number of matings by females (MR, orange) and female fitness (F, green). b Changes in the
proportion of females with twin slots (2S), which started to invade the population at the 1000th generation (the black arrowhead), with schematics
of 1S and 2S states. Solid lines and shaded areas of respective lighter colors show the mean ± SD for 40 runs under the FR (fair raffle) regime
(R = 800, c = 55). c Spermathecal plate (delineated by red dashed line) of Neotrogla truncata with a spermatophore. A female can actively control the
direction of seminal flow (blue arrow), either to slot A (green arrow) or to slot B (purple arrow). Scale bar: 50 µm
and Kamimura [29] demonstrated that female-biased sex
ratios promote the production of smaller ejaculate packages by males in order to mate with more females. Doubling the slot number can have a similar effect on male
ejaculate allocation. Thus, for comparison to this invasion experiment (doubling-slot [DS] runs), the number
of females was doubled, resulting in male:female = 1:2,
from the mid (the 1000th generation) of simulation runs
and beyond in “doubling females [DF]” runs. Neither
the numbers of slots nor females were doubled throughout the 2000-generation runs in the control runs (CON:
Table 1).
Figure 5 clearly shows that 2S females successfully
invaded into a population when females could not
satisfy their required number of matings on average
(Fig. 5). Such a condition occurs (1) when mating costs
for females are extremely low and the environment is
oligotrophic regardless of the paternity determination
regimes, or (2) when males evolve large-sized gifts,
reception of which is beneficial for females and outweighs the associated mating costs (Fig. 4A, C).
Under these conditions, 2s genes for making the twin
slots usually increased rapidly and became fixed (being
95% or more) in the population (Fig. 3a, b). Prevalence
of 2S females caused a coevolutionary reduction in
male gift size (Fig. 3a, b). Accordingly, females needed
an increased number of matings to approach their fitness optimum, resulting in a reduction in their average
fitness (Fig. 6). When mating cost was relatively low,
females could not satisfy their demands even with an
increase in mating frequency by possessing two slots.
However, with a higher mating cost and especially in
eutrophic habitats, the smaller sized gifts, as a male
counter-adaptation to twin slots, became unattractive
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Page 7 of 14
to the females, resulting in a higher satisfaction rate
(compare Fig. 5A-c with 5A-a).
Strikingly similar patterns were observed when the
number of females was doubled at the middle of simulation runs (Fig. 6a; Additional file 1). However, under
each parameter set, the observed reduction in fitness was
less prominent when 2S females were fixed compared
to when the female number was doubled (Fig. 6a), while
among-individual variations in female fitness (measured
as SDs) were comparable, being higher than the controls
(Fig. 6b; see also Additional file 3).
Discussion
Evolution of nuptial gifts: relevance to empirical studies
Fig. 4 Average male seminal gift size (V, light blue backgrounds) and
the realized number of matings by females (MR, pink backgrounds)
at the 2000th generation observed in the control runs (CON) of four
different paternity-determination regimes (A FR [fair raffle]; B ES
[equal shares]; C LM [complete last male]; and D FM [complete first
male])
Fig. 5 Average satisfaction rate (MR/MO) of female mating demands
in CON [control] (a) and DS [twin-slots invasion] (c) runs, and
proportion of 2S females (b) in DS runs at the 2000th generation (A
FR [fair raffle]; B ES [equal shares]; C LM [complete last male]; and D
FM [complete first male]). The asterisks in A‑b indicate the parameter
sets examined in Fig. 6
Our simulation revealed that when mating costs for
females are extremely low in oligotrophic environments
(low R plus low c), females cannot satisfy their demands
for male derived nutrients regardless of the paternity
determination regimes (Fig. 5a). This result supports the
view that scarcity of other nutritive sources for female
reproduction can be a favorable factor for the evolution
of high dependency on male-derived gifts [16, 30]. The
paternity-determination regimes also show complicated
interactions with these environmental/ecological factors in determining the coevolutionary feedbacks. Except
for “low R plus low c” conditions discussed above, both
female traits, high mating rates and twin-slots, rarely
evolved in the ES (equal shares) and FM (complete first
male) regimes. In the LM (complete last male) regime,
males evolved gigantic gifts almost exclusively when their
donation results in monandry, supporting the view that
male control over female remating rate may be responsible for the origin of nutritious ejaculates in some cases
[10, 31]. A high positive correlation between male seminal expenditure and the resultant paternity is a requisite
for the evolution of effective nuptial gifts coupled with
female polyandry for obtaining the gifts under a wide
variety of R and c (the fair raffle [FR] regime; Fig. 5).
These results provide important insights into the difficulty in discriminating the “mating effort” and “paternal
investment” hypotheses (see “Background”). Nutritious
nuptial gifts are effective as male mating efforts when
females compete to accept (additional) matings to obtain
them. The present study revealed that such effective
nuptial gifts evolve almost exclusively when donation of
large-sized gifts results in high paternity gains, measured
as the number of offspring nourished by the female (the
FR or LM regime). In these cases, nourishing females
as mating efforts by males inevitably results in a higher
paternal investment on average.
Although male paternity share is unknown for most
animal taxa with nuptial gifts at present, positive correlation between gift size and male paternity share (or the
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Page 8 of 14
Fig. 6 Box plots of the average female fitness (a), SD of female fitness (b), and average male gift size (c) observed at the 2000th generation under
the FR regime. Results for four different parameter sets, indicated by the asterisks in Fig. 5A-b and the three different simulation modes (CON,
control; DS, twin-slots invasion; DF, double the number of females) are shown
number of sperm stored) has been reported for several
cases [13, 15, 32–35]. Among them, in the hangingfly
Hylobittacus apicalis (Mecoptera: Bittacidae), females
accept mating only while eating a nuptial gift (small
arthropod prey) donated by the male. Their narrow
and elongated spermathecal duct disturbs rapid sperm
transfer from males. Therefore, only males who offer a
large prey item are allowed to transfer enough sperm to
assure their paternity [36]. Similar morphology has been
reported for some other insect taxa with nuptial gifts [37,
38].
To keep our model simple, we did not incorporate the
following pivotal factors that are known to affect trading of nuptial gifts: assessment of gift size by females
before receiving the gift (and deception of gift size by
male donors), strategic modulation of gift size by males
based on mating status of mates (e.g., unmated vs. previously mated females), and costs of mating itself for males
Kamimura et al. BMC Ecol Evo
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[reviewed in 1,2,5,13,32]. If a large-sized gift attracts
more females, exaggeration in gift size may also occur
under almost complete first male sperm precedence. For
Neotrogla spp., in which copulation with the female positioned above the male lasts for a long period (see “Background”), male mating costs can be especially relevant. In
addition, seminal gift size can also vary interspecifically
through possible macro-evolutionary trade-offs with
other male and female traits: donation of anti-aphrodisiac components to females in crickets [39], male calling
frequency in bushcrickets [40], male weaponry in megalopteran insects [41], and male bioluminescent courtship
and female flightlessness in fireflies [33, 42–44]. These
complexities should be taken into account when comparing theoretical predictions with empirical data.
Evolution of female morphology for gift‑acquisition
Like all other members of the tribe Sensitibillini known
to date, Neotrogla spp. exclusively occur in oligotrophic,
dry cave habitats (low R: [45, 46]). In addition, they retain
ancestral “female above male” mating positions (Fig. 2),
suggesting that males do not impose high mating costs
on females (low c). However, they are apparently polyandrous as evidenced by multiple emptied spermatophore
capsules, the volume of which corresponds to ~ 300 ml
if scaled up to human proportions [23], in their spermatheca [22]. In our model, such a combination of female
multiple mating and large-sized gifts occurred only in the
fair raffle (FR) regime (Fig. 4). Though sperm usage/storage patterns are completely unknown at present for the
members of Sensitibillini, their spermathecal duct (sperm
corridor) is especially elongated and coiled among Psocodea (booklice, barklice, and parasitic lice) [24, 46–50].
Thus, it is plausible that the narrow and extremely long
sperm corridor of Sensitibillini also functions to establish a positive correlation between seminal gift size and
transferred sperm number (FR regime). Since many
psocids show continuous production and deposition of
eggs after sexual maturity [51, 52], the LM (complete last
male) regime is also a candidate if females mate with a
single male in each oviposition interval. Although some
Neotrogla females possess two freshly deposited spermatophores attached to the twin-slots [22], it is presently
unknown whether they are derived from two different
males. Future studies should clarify sperm usage patterns
in this unique group of insects.
Our simulations also demonstrated that twin slots
for obtaining gifts in rapid succession are advantageous
when females cannot achieve their required number of
matings, and that the evolution of this persistence trait
has notable effects on the coevolutionary dynamics in
trading of nuptial gifts between the sexes. Little is known
about the transitional process from the single-slot state,
Page 9 of 14
which certainly is ancestral in psocids, to the twin slots
observed uniquely in Sensitibillini. For simplicity, we
assumed that single-slot and twin-slots states can be
switched by two alleles of a single locus. However, since
the spermathecal plate of the extant Sensitibillini is a
complex structure harboring not only the twin slots for
seminal gifts, but also a muscle-driven mechanism to
switch seminal flows between them [23; Fig. 3c], it has
likely evolved gradually from primitive precursors during
its long evolutionary history of approximately 50 million
years (from 177.5 Mya to 127.2 Mya: [53]).
Unlike doubling the female number, the evolution of
twin slots usually resulted in less pronounced reduction in female fitness with its comparatively large variance (Fig. 6). A larger variation in the female fitness
means stronger sexual selection operating among them.
This intensified female-female competition for malederived nutrients, caused by the evolution of twin slots,
could also be a crucial factor favoring the evolution of a
manipulative intromittent organ in the female Sensitibillini. Interestingly, detailed comparative morphology
and molecular phylogeny of Sensitibillini indicated that
a female penis with an intromittent function has evolved
twice independently, in Neotrogla and Afrotrogla, in this
small insect tribe [28, 45, 54], although the detailed genital functions of Afrotrogla are still unknown.
As a coevolutionary response for filling the increased
number of slots, males reduce the size of each gift, resulting in an increase in the optimal number of matings for
females. Persistence traits, such as genital spines for
anchoring unwilling mates or intromittent organs for
traumatic insemination, usually develop in males, and can
reduce the total fitness of their mates [55, 56]. Theoretical studies show that this kind of inconsistency between
male and female interests can even result in a high risk of
extinction, driven by the evolution of male “selfish” traits
for escalated male-male competition for mates [57]. This
type of trait can also be exaggerated through arms races
between the sexes so that females also develop counteradaptations to resist or tolerate male persistence (sexually antagonistic coevolution; e.g., [58, 59]). The results of
the present study clearly indicate that even “persistence”
traits can be in the category of sex-reversed traits, driven
by the evolution of effective nuptial gifts.
Evolution of nuptial gifts: relevance to previous models
There are only a few preceding studies on the coevolutionary feedbacks between the sexes in trading of ejaculate components. Like nutritious materials in nuptial
gifts, sperm itself can be considered as a limited resource
for both sexes [60–68]. Considering a situation equivalent to the FR (fair raffle) regime of this study, a previous study examined the effects of several environmental
Kamimura et al. BMC Ecol Evo
(2021) 21:164
factors on the evolutionary feedbacks between male
sperm allocation strategies and female mating rate [29].
In the model, increased mating costs for females (cf,
equivalent to our c) resulted in a lower female mating
rate and an increased sperm package size, similar to the
results of the present study. The study also showed that
reduction in resource availability to males (low R) results
in a monotonic reduction in the ejaculate size [29].
Although our present model showed similar dependency
of seminal gift size (V) on R, prudently allocated gifts
were also observed in extremely eutrophic environments
with high female mating costs (Fig. 4A). This difference
can be attributed to the different assumptions adopted:
in the model of Abe and Kamimura [29], a size-number
trade-off in seminal production was assumed only when
females cannot satisfy their demands for sperm supply.
Bocedi and Reid [69] also examined the effects of varying female mating costs on the coevolutionary feedbacks between male sperm traits (sperm number and
sperm longevity) and female mating frequency. Under
fair raffle sperm competition, an increase in female mating costs resulted in reduced polyandry, as seen in the
present study, but also in a reduction of sperm number
transferred during a single mating event [69]. The latter
finding makes a striking contrast to our results in which
males prepare larger gifts for less polyandrous females
unless the environment is not extremely eutrophic
(Fig. 4A). This can also be attributed to the different
assumptions adopted for delineating trade-off relationships: a trade-off between sperm number and sperm longevity was incorporated in Bocedi and Reid [69] instead
of a size-number trade-off. Males should invest more
resources to sperm longevity, rather than sperm number,
when they experience a low sperm competition risk in
less polyandrous females.
Conclusion
The present study has clearly demonstrated that sperm
usage patterns, which have rarely been examined for animals with nuptial gifts, can be a pivotal factor for determining the extent of exaggeration in nuptial gifting. Our
simulation results have shown that female multiple matings for obtaining male-derived gifts always evolve under
oligotrophic environments with low mating costs. However, exaggeration in gift size occurred only under limited conditions: (1) when gift size is positively correlated
with siring success, or (2) when donation of a large gift
imposes monandry under high last-male sperm precedence. When females could not achieve their optimal
number of matings, a persistent female trait for competitively acquiring gifts can further invade. However,
through coevolutionary reduction in male gift size, fixation of this trait can drastically reduce the average female
Page 10 of 14
fitness (i.e., population productivity), as is the case with
sexually persistence traits in males.
Methods
Model assumptions
All notations and parameter values used in this article
are summarized in Table 1. It is likely that a given volume of nuptial gift will increase the female’s fecundity
more effectively when the female is starving than when
she has already received a large amount of nutrients from
the preceding mates. Thus, we assumed that the potential
offspring number of a female (fecundity, FF_pot) is a saturation function of the cumulative volume of seminal gifts
(r) received in all of her previous matings (Fig. 1):
FF_pot (r) = FF_max 1 − e−br
(1)
where b, set at 0.002 throughout the present study, represents the speed of saturation. In this equation, FF_max, set
at 800, denotes the maximum number of offspring that a
female can potentially produce when r = ∞ under no cost
of mating.
Even in cases in which males donate nuptial gifts at
each mating event, multiple mating, which may involve
costly mate-searching and an enhanced risk of being
predated, can be detrimental for the females. Thus, we
imposed a cost (c) for each mating event, as a reduction
in the number of offspring as:
FF (r, c, MR ) = FF_pot (r) − c · MR
(2)
where MR is the number of times a focal female mates.
Since we assumed no differential mortality between genotypes in this study, the fecundity delineated by Eq. 2 is
directly proportional to the female fitness, i.e., the number of reproductives of the next generation. Thus, Eq. 2,
which represents the realized fecundity, was used as the
expected fitness of females.
This simple function delineates complicated coevolutionary relationships between the male and female
traits (Fig. 1). When males donate a large-sized gift at
each mating (e.g., V = 500), an additional mating further
increases the lifetime fitness of a singly-mated female
under a low-cost mating (e.g., c = 100; orange arrows in
Fig. 1), but not when it is largely costly (e.g., c = 200; red
arrows).
We assumed that reception of a gift, which occupy a
slot for its digestion, delays subsequent matings of the
female, in a manner proportional to the gift size. Thus,
from a male perspective, males that produce large-sized
gifts can reduce the probability that a female remates
while increasing their fecundity. However, given a limited amount of resource available for gift production (R),
Kamimura et al. BMC Ecol Evo
(2021) 21:164
Page 11 of 14
males with large V suffer a reduced number of possible
matings (N ≈ R/V; a size-number trade-off ).
We examined four different regimes for the relationship
between the nuptial gift size and the resultant paternity
gain in this study: (1) fair raffle (FR), (2) equal shares (ES),
(3) complete last male (LM), and (4) complete first male
(FM) (Fig. 2, Table 1). In the case that males can transfer
more sperm by giving a large-sized gift (the FR regime), it
can result in a higher paternity share compared to males
who gave a smaller gift to the same mate.
Given these assumptions, the expected fitness of a male
(FM) that donated a total of n (n ≤ N) gifts to females can
be written as:
FM (V ) =
n
Pi FFi
(3)
i=1
where Pi and FFi are the paternity share and the realized
fecundity (= expected fitness given by Eq. 2) of the female
that received the ith gift from the focal male. Under the
ES (equal shares) paternity determination regime, Pi is
1/MR if the female mate MR times before offspring production. It is 1 (0) or 0 (1) when the focal male is the first
(last) male of a mate or not, under the complete first
male (FM) (complete last male [LM]) regime, respectively. However, the probability for being the first (or last)
male depends on both the gift size of the focal male (Vfocal) and those of MR rival males, requiring an individualbased simulation approach for solving the coevolutionary
dynamics. It is also true for the fair raffle (FR) regime, in
which Pi is given as:
Pi = Vfocal /
MR
Vj = Vfocal /r
(4)
j=1
Simulation details
Individual-based simulations were conducted to observe
the coevolutionary dynamics of three traits: male seminal
gift size, female propensity for multiple mating, and the
number of slots for obtaining gifts in females. For this,
we used a personal script written in Python 3.7.1, which
is provided as Additional file 4. Simulations were run for
2000 generations assuming a single population of diploid
organisms with sexual reproduction and discrete generations. The population size was set at 1000 (500 males
and 500 females). Nuptial gift size, a trait of male-specific expression, was assumed to be determined by many
alleles. To mimic sexual reproduction, we assumed a single locus with infinitely many possible alleles for this trait
(continuum of alleles model). The initial value for each
gene was randomly extracted from a normal distribution,
with a mean of 20 and a standard deviation (SD) of 40.
Each individual possesses two values, v1 and v2, as the
genotype of this trait. The seminal gift size (volume; V)
was determined as (v1 + v2)/2 only for male individuals
as their phenotype. Similarly, a mean of 0.5 ± 2 was given
as the initial values for the propensity for multiple mating
(m1 and m2), which determines the maximum number of
“additional” matings accepted by each female individual
(M), as the nearest integer of (m1 + m2)/2. Thus, females
of the genotype m1/m2 mate M + 1 times, whenever a
mating opportunity is available. To prevent the occurrence of unreasonable values in these two traits, we set
the lower limits of genetic values of these two traits as 20
and 0, respectively.
Another female trait, the number of slots for accepting nuptial gifts, was assumed to be a dichotomous trait,
that is, one or two slots. Little is known about the evolutionary process of the spermathecal plate, which enables
retention of two nuptial gifts simultaneously (see "Discussion”). For simplicity, we assumed that the transition is
controlled by a single locus with two alleles: 2s, a gene for
the twin-slot state, and 1s, a gene for the single-slot state,
the former was assumed to be dominant over the latter.
The populations were initiated with single-slot females
(1S, 1s/1s homozygotes). Then, 2s genes were allowed
to invade to populations at the 1000th generation and
beyond (one spontaneous mutation in each generation),
together with recurrent invasion of single-slot mutants
(a female individual of 1s/1s homozygote per generation)
to check the evolutionary stability of the twin-slot state
(2S). When the 2S phenotype occupied 95% or more of
females, this phenotype was judged as fixed.
In the model, each male can mate up to N times, which
is R/V rounded up to the nearest integer, where R is a
total volume of resource available for production of nuptial gifts, randomly extracted from a normal distribution.
The gift size of the last mating (Vlast) is:
Vlast = R − (N − 1)V
(5)
The mean value of R ranged from 400 to 1300, by increments of 100, representing an environmental variability
in resource availability (oligotrophic to eutrophic). The
SD was set at each mean value multiplied by 0.2.
In our model, we considered only the effects of postcopulatory sexual selection on the coevolution between
male gift size and female traits for obtaining gifts. Any
precopulatory behaviors, such as male-male combats for
mates or female choice on gift size or males, were not
incorporated. For implementing this condition, seminal gifts produced by all male individuals were pooled
and considered as mating opportunities in every generation. Males producing many small gifts represent
a larger proportion of this “gift pool”, incorporating the
size-number trade-off specified above. We assumed that
Kamimura et al. BMC Ecol Evo
(2021) 21:164
all virgin females start to mate simultaneously, by randomly assigning a gift from the pool to a slot. This procedure guarantees that all females mate at least once, unless
the sex ratio is female-biased (doubled: see below) and
males produce only a few gifts (less than two on average)
per capita. A female accepts additional mating when (1)
she has mated fewer times than her acceptable number
of matings (M + 1), and (2) at least one of her slots are
empty. Remaining seminal gifts in the pool were then
sequentially assigned, one at a time, to the slot that had
received the minimum cumulative volume of gifts (r) in
females whose mating demand was not satisfied at the
time. Thus, reception of a large gift, which is difficult to
digest for females, resulted in delayed remating of the
female. This procedure was repeated until all females
satisfied their mating demands, or the gift pool became
empty (= all males exhausted their resource budgets).
Then, the expected fecundity of each female (F) was
calculated according to Eq. 2. Cost of mating, defined by
a reduction in female fitness per mating (Fig. 1), was varied from 5 to 95, by increments of 10, and negative fitness values were treated as zero. To keep the constant
population size, maternity and paternity of offspring
were determined stochastically according to the proportional representation of the relative fitness of females
(Eq. 2) and the relative representation of male sperm in
each female (Pi of Eq. 3), respectively. For each trait, one
of two parental genes was randomly and independently
extracted from two parents, and fused to create an individual of the next generation, that is, with no linkage
among the three traits. For seminal gift size and propensity for female multiple mating, each of these values was
treated as the mean of a normal distribution for creating
the genetic values of progenies (recurrent mutation) with
SDs 40 or 2, respectively.
To dissect the complicated coevolutionary interactions
between the male and female traits, simulations were
repeated 40 times for each combination of R and c values,
and for each of the four different paternity determination
regimes (FR, ES, LM, and FM) specified above (Fig. 2). In
addition, three different types of simulations were conducted (Table 1). Abe and Kamimura [29] demonstrated
that female-biased sex ratios promote the production
of smaller ejaculate packages by males in order to mate
with more females. Doubling the slot number can have a
similar effect on male ejaculate allocation. For comparison with doubling-slot (DS) runs, in which one twin-slot
mutant female (2S female) was introduced every generation after the 1000th generation, the number of females
was doubled, resulting in 1000 females per 500 males,
from the 1000th generation and beyond in doubling
females (DF) runs. In the control runs (CON), neither the
numbers of slots nor females were doubled throughout
Page 12 of 14
the 2000-generation runs. Possible effects of genetic
correlation between the male and female traits on their
coevolution were also examined (see Additional file 2).
Supplementary Information
The online version contains supplementary material available at https://doi.
org/10.1186/s12862-021-01901-x.
Additional file 1. Examples of the coevolutionary dynamics between
the male seminal gift size and optimal number of matings for females
observed in CON (control) and DF (doubling females) runs.
Additional file 2. Examination of genetic correlation between the male
seminal gift size and optimal number of matings for females.
Additional file 3. Comparisons of relative intensity of sexual selection
between the sexes.
Additional file 4. Model source code written in Python 3.7.1.
Acknowledgements
We thank two anonymous referees for their helpful comments on previous
versions of the manuscript.
Authors’ contributions
YK, JA and KY conceived and coordinated the project; YK wrote scripts, conducted simulation, and analyzed data; KY, CL, and RLF discussed relations to
empirical data; and all authors wrote the paper. All authors read and approved
the final manuscript.
Funding
This study was partly supported by the Japan Society for the Promotion of
Science research grant 15H04409 to K.Y. and Y.K., 17K07574 to J.A., 19K06746
to YK, and The National Council for Scientific and Technological Development
(Brazil) CNPq Grant n. 308334/2018-3 to R.L.F.
Availability of data and materials
All data was generated by the Pyhton script, which is provided as Additional
file 4. All data is deposited in in the Dryad Digital Repository: https://doi.org/
10.5061/dryad.n5tb2rbtc.
Declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Author details
1
Department of Biology, Keio University, Yokohama 223-8521, Japan.
2
Systematic Entomology, School of Agriculture, Hokkaido University,
Sapporo 060-8589, Japan. 3 Geneva Natural History Museum, CP 6434,
1211 Geneva 6, Switzerland. 4 Biology Department, Federal University of Lavras,
Lavras, MG 37200-000, Brazil. 5 Faculty of Liberal Arts, Meijigakuin University,
Yokohama, Japan.
Received: 29 March 2021 Accepted: 19 August 2021
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