Sex ratio in the mother's environment affects offspring population dynamics: maternal effects on population regulation

Abstract

Classic population regulation theories usually concern the influence of immediate factors on current populations, but studies investigating the effect of parental environment factors on their offspring populations are scarce. The maternal environments can affect offspring life-history traits across generations, which may affect population dynamics and be a mechanism of population regulation. In cyclical parthenogens, sexual reproduction is typically linked with dormancy, thereby providing a negative feedback to population growth. In this study, we manipulated population sex ratios in the mother's environment to investigate whether this factor affected future population dynamics by regulating offspring sexual reproduction in the rotifer Brachionus calyciflorus. Compared with females in male-biased environments, those in female-biased environments produced fewer mictic (sexual) offspring, and their amictic (asexual) offspring also produced a lower proportion of mictic females at a gradient of population densities. Moreover, populations that were manipulated under male-biased conditions showed significantly smaller population sizes than those under female-biased conditions. Our results indicated that in cyclical parthenogens, mothers could adjust the sexual reproduction of their offspring in response to the current population sex ratio, thus providing fine-scale regulation of population dynamics in addition to population density.

1. Introduction

Identification of the potential mechanisms underlying population regulation is essential to understand and predict processes of population dynamics. Classic population regulation theories, including those that take extrinsic or intrinsic factors of a population as the main population regulators, mainly concern the influence of immediate factors on the current generation [1–3]. Maternal effects can transmit environmental conditions across generations [4,5] and affect offspring performance directly by changing offspring life-history traits [6–8] or indirectly by influencing their environment [9]. Recent studies have reported that maternal environment and phenotype can affect trade-offs between offspring size, number [10], quality [4,11], survival and reproduction [12,13], which in turn affect population growth [14,15]. For example, Bian et al. [13] found that in root voles (Microtus oeconomus), when mothers experienced a higher population density, they produced offspring with higher corticosterone metabolite levels and lower reproductive capacity, and the sizes of the subsequent populations founded by these offspring were also lower. Therefore, maternal effects could be an important factor for explaining population dynamics.

For cyclically parthenogenetic rotifers (monogonont rotifers), asexual and sexual reproduction alternatively occur throughout life [16,17]. During the asexual phase, amictic (asexual) females typically produce offspring asexually and sequentially, which permits rapid population growth of clones [18]. Sexual reproduction is initiated when some amictic females occasionally produce sexual offspring (also known as mictic females) as a fraction of their offspring. Young mictic females have two mutually exclusive reproductive fates: if they are fertilized by males within a threshold age, they produce diploid resting eggs in their lifetime, which usually undergo obligate diapause for weeks to months before hatching [19], while unfertilized mictic females produce haploid eggs in their lifetime, which develop parthenogenetically into males. Due to the demographic costs of sexual reproduction compared to asexual reproduction in an actively growing population [20–24], the induction of sexual reproduction could be a critical determinant of population dynamics [20,21]. We already know many environmental and endogenous factors controlling the initiation of sexual reproduction; among these factors, population density is the best-known ecological and evolutionary predictor for sexual reproduction [25–27].

However, in monogonont rotifers and other cyclical parthenogens, sexual reproduction concerns not only which reproductive mode to invest in (sexual or asexual) but also which sex of offspring to produce, as investment in the sexual mode might result in low fecundity of resting eggs when fertilization rates are low, due to a reduced chance of successful reproduction. The population sex ratio could fluctuate over time with population demography and/or environmental changes (electronic supplementary material, figure S8), causing the relative reproductive values of producing males or females to vary. Fisher's sex allocation theory explains an even allocation of resources to male and female function by a negative frequency-dependent selection [28]. Trivers & Willard [29] hypothesized that when reproductive success differs between sons and daughters, it is adaptive for mothers to produce offspring of the sex that yields the highest fitness benefit. In monogonont rotifers, male-producing mictic females (hereafter, MMFs) indirectly account for sex allocation to males because they are equivalent to sexual males, and resting egg-producing mictic females (hereafter, RMFs) indirectly account for sex allocation to females because they are equivalent to sexual females; consequently, the sex allocation ratio is defined as the proportion of male-producing sexual females in relation to the total abundance of sexual females $\mathrm{MMF}/(\mathrm{MMF}+\mathrm{RMF})$ [30,31]. In the rotifer B. calyciflorus, male abundance affects sex determination in a negative frequency-dependent process: the lower the density of males, the lower the insemination rate and the higher the density of MMFs, which in turn elevates the subsequent fertilization rates and the frequency of RMFs. However, whether rotifer mothers can respond to the sex ratios of the current population and alter investment in sexual reproduction is still unknown. Research on this problem could improve understanding of the induction of sexual reproduction and its consequences on population dynamics in the context of the population sex ratio.

In the present study, we aim to illustrate how the population sex ratio in the mother's environment is related to population regulation with the rotifer B. calyciflorus as a model animal. We predict that when the population is MMF-biased, amictic mothers will produce a higher proportion of mictic offspring; when the population reaches an RMF-biased sex ratio, mothers will reduce the proportion of mictic offspring. Due to the demographic cost of sexual reproduction, MMF-biased populations will reach a lower population size than RMF-biased populations. In such cases, variation in population sex ratio in the mother's environment will have a population dynamic consequence.

2. Methods

(a) . Rotifer culture

The rotifer B. calyciflorus was originally collected from a freshwater pond in Beijing, China (39°57′ N; 116°21′ E) and reared in our laboratory for 1 year to establish a laboratory population. The clonal populations used here were built by hatching a resting egg collected by a laboratory population that has been genetically marked (accession number of COI sequence in GenBank: MK344674). Before the experiments, rotifer populations were cultured at a density of 0.025 ind ml⁻¹ in COMBO medium [32] with Chlorella pyrenoidosa [33] as food (1 × 10⁶ cells ml⁻¹) at 20°C (light : dark 16 : 8). Chlorella pyrenoidosa was cultured in SE medium [33] at a constant photoperiod (3000 lux) and 25°C. Culturing medium was refreshed every 2 days with fresh foods.

(b) . Preparation of conditioned medium with different sex ratios

In the present study, the sex ratio was defined as the proportion of MMFs in all mictic females, which was measured as $\mathrm{sex}\hspace{0.17em}\mathrm{ratio}=\mathrm{MMF}/(\mathrm{MMF}+\mathrm{RMF})$. Our previous experimental results showed that conditioned COMBO medium with cues of different ratios of MMFs (equivalent males) versus RMFs (equivalent females) could alter amictic mothers' propensity to produce mictic offspring (WJ Li 2018, unpublished data). In the present study, when stock populations were in the exponential growth phase, 100 newly matured MMFs or RMFs were randomly collected from the stock populations and cultured in 50 ml COMBO medium without food for 24 h. The conditioned media of each sex were filtered through 0.5 µm glass fibres and then blended to the experimental population sex ratio levels, while the population density cue of the conditioned medium was held constant. The conditioned medium of each treatment with three replicates was created and refreshed daily.

(c) . Experimental design

Three experiments were conducted to test the effects of population sex ratios in the mother's environment on offspring sexual reproduction and on population dynamics.

Experiment 1: Effects of the population sex ratio in the mother's environment on the proportion of mictic daughters.

Newly born amictic females (F₀) were randomly picked and assigned to single wells of 24-well plastic plates (Costar-3524, Corning, Inc., USA) with 2 ml of conditioned medium with sex ratio cues ranging from 0 to 1 (0.00, 0.25, 0.50, 0.75 and 1.00) containing food (C. pyrenoidosa, 1 × 10⁶ cells ml⁻¹). In each sex ratio level treatment, there were 24 F₀ female replicates that received the same volume and concentration of conditioned medium. Media were refreshed every 24 h. When offspring (F₁) from each F₀ group were born, they were all immediately collected. Birth order was recorded, and offspring (F₁) were cultured individually in COMBO medium with food until the female type could be identified under a dissecting microscope. Then, the mixis ratios (investment in sexual reproduction) ($\text{mixis ratio}=$ mictic offspring/mictic offspring + amictic offspring) of all F₁ individuals from each F₀ were computed by the sex ratio level (the experimental procedure is shown in electronic supplementary material, figure S2A).

Experiment 2: Effects of the population sex ratio in the mother's environment on the offspring's response to population density.

Newly born amictic females (F₀) were randomly picked and assigned to single wells of 24-well plates with 2 ml of conditioned medium containing cues of sex ratio of 0.15 (LSR treatment) or 0.85 (HSR treatment) (our previous experiments showed that 1 day after the RMF emerged, the population sex ratio was approximately 0.85 and when the population size reached a peak, the sex ratio was approximately 0.15) with food (C. pyrenoidosa, 1 × 10⁶ cells ml⁻¹). The females were cultured under this condition until the first amictic daughter (F₁) was born. Newly born amictic F₁ females from each sex ratio group were immediately picked out and cultured individually in different medium volumes (40, 20, 10, 5, 2 and 1 ml) to create six population density levels (0.025, 0.05, 0.10, 0.20, 0.50 and 1.00 ind ml⁻¹) [28] and cultured until they died. Every day, F₁ amictic females in each density treatment were transferred to fresh medium. All daughters (F₂) of each F₁ female were collected, birth order was recorded and daughters (F₂) were cultured singly in 1 ml COMBO medium with food in 24-well tissue culture plates until they could be typed as amictic or mictic. Then, the mixis ratios of all F₂ offspring from each F₁ female were computed (the experimental procedure is shown in electronic supplementary material, figure S2B). The number of replicate females (F₁) per density treatment ranged from 17 to 24.

Experiment 3: Effects of the population sex ratio in the mother's environment on population dynamics.

Three treatments including 18 replicate populations were established with young amictic females arbitrarily sampled from the stock populations at an initial density of 1 ind ml⁻¹ in six-well plastic plates with 10 ml of COMBO medium containing food (C. pyrenoidosa, 1 × 10⁶ cells ml⁻¹). Replicates in one treatment were evenly divided into different plates. All animals in each replicate were transferred to a fresh medium containing food daily. Meanwhile, the density and demographic structure of each population were recorded under a dissecting microscope. Population samples were categorized by reproductive status and egg types: juvenile females; reproductively matured females, which were further classified as amictic females (carrying large, diploid eggs developing into females, electronic supplementary material, figure S1A); MMF (carrying much smaller eggs that develop into diminutive males, electronic supplementary material, figure S1B); RMF (carrying large, dark colour, resting eggs, electronic supplementary material, figure S1C). From day 5 onwards (the first day when RMFs appeared in the treatment population, MMFs usually appeared 1–2 days earlier than RMFs), six replicate populations were manipulated by replacing all MMFs in the populations with RMFs (i.e. low population sex ratio treatment, hereafter LASR), six replicate populations were manipulated by replacing all RMFs in the populations with MMFs (i.e. high population sex ratio treatment, hereafter HASR), and this manipulation was repeated until the end of the experiment. The remaining six replicate populations served as the control populations (control treatment) without replacement. The above manipulation was performed to create a constant difference in the population sex ratio among the three treatments. Both MMFs and RMFs used in replacement were obtained from supplemental populations cultured at a population density of 4–5 ind ml⁻¹ in 1500 ml medium in three 2000 ml glass dishes, and the rearing medium with food was changed daily. The experiment continued for 15 days until the control group had experienced two population size peaks.

(d) . Statistical analysis

Mixis ratios were calculated to evaluate the investment in sexual reproduction. Data are presented as the mean ± standard error (s.e.). To test effects of the population sex ratio in the mother's environment on its investment in sexual reproduction and offspring number, we conducted one-way ANOVA with the population sex ratio in the mother's environment as a fixed-effect factor.

In the second experiment, population sex ratios in the environment of F₀ mothers, population densities of F₁ females and their interaction were set as fixed factors, and their effects on the propensities of F₁ females to produce mictic daughters (F₂) were analysed by a generalized linear model (GLM) (family = quasi-Poisson). Thereafter, Tukey's HSD test was conducted to compare the means among different treatments.

In the third experiment, we ran a linear mixed model (LMM) to determine whether the population sex ratio treatments could affect population dynamics. In this model, we included the daily population sizes as response variables and treatments and days as explanatory variables. Replicates within each treatment were included as a random factor. To analyse the effect of the population sex ratio and population density on the mixis ratio of populations, we used daily population density, population sex ratio and population mixis ratio data from the control treatments. We ran a LMM including population density and population sex ratio as fixed factors. Replicates were included as a random factor. The significance level was set at p < 0.05. All statistical analyses were carried out using the statistical package R v. 4.0.3 (R Core Team 2020). Figures were drawn by Origin Pro v. 9.0.

3. Results

(a) . Effects of the population sex ratio in the mother's environment on the offspring mixis ratio and offspring number

When mothers were cultured at the lowest population sex ratio of 0.00, the offspring mixis ratio was also the lowest; by contrast, mothers from the high sex ratio treatment produced a higher proportion of sexual offspring (F_4,109 = 16.712, p < 0.001; figure 1). However, mothers from different population sex ratio treatments showed no significant differences in the average number of offspring they produced (F₄,₁₁₂ = 1.647, p = 0.167; electronic supplementary material, figure S3).

Figure 1.

Effects of the population sex ratio in the mother's environment (F₀) on the proportion of mictic offspring (F₁). The solid horizontal line is the median, the dot is the mean, the deviation bars represent the 10th and 90th percentiles and asterisks show the maximum and minimum values. No common superscript letters show significant differences in the proportion of mictic offspring of F₀, and the significance level is set at p < 0.05.

(b) . Effects of the population sex ratio in the mother's environment on the offspring's response to population density

Both the maternal (F₀) population sex ratios and population density of F₁ females significantly influenced the mixis ratios of the F₂ generation, and there was a significant interaction (table 1). In the HSR treatment, the proportions of mictic daughters of F₁ females all increased significantly along an increasing gradient of population densities (table 2). However, when F₁ females were from mothers who had experienced a LSR, the mixis ratio of the F₂ generation did not vary with population density and was dampened (figure 2 and table 2). At all population density levels, the average mixis ratio of the F₂ generation was the lowest in the LSR treatment (figure 2 and table 2), even at the highest population density (1 ind ml⁻¹), with a mixis ratio of 16.565% (table 2), which was significantly lower than those of the HSR treatments (table 2).

Table 1.

Effects of the population sex ratio in the environment of F₀ and population density in F₁ on the proportion of mictic offspring (F₂) of F₁ females estimated by a GLM (family = quasi-Poisson).

source	estimate	s.e.	t-value	Pr(>|t|)
intercept	2.830	0.083	33.935	<0.001
population sex ratio in F0 (A)	0.359	0.034	10.691	<0.001
population densities of F1 (B)	−0.00042	1.793 × 10−4	−2.358	0.0188
A × B	0.00024	6.985 × 10−5	3.528	<0.001

Table 2.

Effects of the population sex ratio in the mother's (F₀) environment on the proportion of mictic offspring (F₂) of F₁ individuals that are cultured across a gradient of population densities. Data are shown as the mean ± s.e. References to HSR and LSR are provided in the Methods. Data with no common superscript letters indicate significant differences between population sex ratios/among population densities. The significance level is set at p < 0.05.

population densities of F1 (ind ml−1)	HSR	LSR
25	33.035 ± 3.414 (a/c)	20.197 ± 3.264 (b/a)
50	33.853 ± 3.919 (a/bc)	27.807 ± 2.825 (ab/a)
100	43.233 ± 3.695 (a/ab)	19.680 ± 2.286 (b/a)
200	37.243 ± 4.653 (a/bc)	22.420 ± 1.977 (b/a)
500	55.671 ± 4.449 (a/a)	18.905 ± 1.741 (b/a)
1000	40.106 ± 2.796 (a/bc)	16.565 ± 1.843 (b/a)

Figure 2.

Effects of the population sex ratio in the mother's environment (F₀) on the proportion of mictic females (F₂) produced by F₁ individuals who were cultured across a gradient of population densities. The open circles represent that the F₁ individuals were from mothers who experienced female-biased treatment (population sex ratio was 0.15, LSR), and the closed circles represent that the F₁ individuals were from mothers who experienced male-biased treatment (population sex ratio was 0.85, HSR). Data are shown as the means ± s.e. No common letters above the error bars indicate means that are significantly different from each other. The significance level is set at p < 0.05.

(c) . Effects of the population sex ratio in the mother's environment on offspring population dynamics

Different fluctuations in population size were observed among populations with different manipulated population sex ratios (figure 3). All populations showed an increase until they reached population densities of approximately 5 ind ml⁻¹. Then, the populations started declining until day 8, when population densities reached a relatively low level. Populations in the female-biased treatment recovered quickly from the decline compared with the other two treatments. Populations in the male-biased treatment remained at a low population size and gradually decreased until the end of the experiment. The maximum population density among the treatments was the highest in the female-biased treatment. Throughout the 15-day experiment, the population densities of the control treatment were significantly lower than those of the female-biased treatment (LMM: estimate = 0.627, se = 0.217, t = 2.886, p = 0.004) but higher than those of the male-biased treatment (LMM: estimate = −1.058, s.e. = 0.217, t = -4.871, p < 0.001). Interestingly, since the 12th day, populations in the female-biased treatment were maintained at a high population density, while those of the other two treatments began declining (figure 3).

Figure 3.

Population density of the three treatments. Open circles represent the control group (control); filled squares represent the treatment where MMFs were replaced with RMFs (LASR); filled circles represent the treatment where RMFs were replaced with MMFs (HASR). Replacement was performed since day 5. Error bars show the mean ± s.e.

In the control treatments, the daily population density, population sex ratio and their interaction significantly affected the daily mixis ratio in the populations (table 3). The population mixis ratio increased when the population sex ratio was more male-biased (figure 4; electronic supplementary material, figure S7). However, the effects of population density on population mixis ratio were altered by the population sex ratio: when the population was more female biased (population sex ratio less than 0.2), the population mixis ratio did not increase with population density; when the population was more male-biased (population sex ratio >0.6), the population mixis ratio was larger than 0.4 and increased with population density (figure 4).

Table 3.

Effects of population density and sex ratio on the mixis ratio in populations from the control treatments estimated by a LMM with population density and sex ratio as fixed factors.

source	estimate	s.e.	t-value	Pr(>|t|)
intercept	0.279	0.045	6.198	<0.0001
population density	−0.011	0.006	−1.992	0.0476
population sex ratio	0.354	0.077	4.618	<0.0001
population density × population sex ratio	0.167	0.036	4.599	<0.0001
random effects				s.d.
				0.107

Figure 4.

Effects of population density and population sex ratio on the population mixis ratio in populations from the control treatments. Different values of the population mixis ratio are shown in gradient colours.

4. Discussion

Sexual reproduction is a critical fitness component in cyclical parthenogens, as sexual reproduction and resting egg formation are tightly linked. Reproducing sexually reflects the trade-off between population growth within a single growing season and population survival among growing seasons [34]. In the present study, we found that the population sex ratio in the mother's environment significantly affected the sexual investment of the next generation, and this maternal effect could significantly alter population dynamics. These findings confirmed an important role of maternal effects in population regulation by changing offspring traits related to population growth.

In monogonont rotifers, sexual reproduction is generally induced by specific environmental cues, e.g. population density is a well-known cue [29–31]. Sexual reproduction is generally hypothesized to occur at high population densities to achieve high fertilization rates of sexual females, as the male–female encounter rates would be high [17,35,36]. However, population densities are not necessarily correlated with fertilization opportunities. Serra et al. [37] hypothesized that sexual reproduction should begin when more sexual females could be fertilized to produce resting eggs. In alignment with this hypothesis, we found that amictic females from male-biased treatment were more likely to produce mictic daughters (figure 1). The population density of mothers in each population sex ratio treatment was controlled at the same level in our experiments; therefore, it is reasonable to conclude that the differences in sexual reproduction were most likely induced by variations in the population sex ratio in the mother's environment.

A high sex ratio in rotifer B. calyciflorus populations indicates a high proportion of MMFs and, consequently, high male abundance; thus, the newly born mictic females are much more likely to be fertilized to produce resting eggs. This is in line with a previous study of sex allocation in another well-studied cyclical parthenogen, Daphnia, which demonstrated that the current population sex ratio provided a reliable cue for mothers to adjust the offspring sex ratio [38]. However, unlike Daphnia, in which females responded to the current sex ratio by directly adjusting the production of ephippia or males, rotifer B. calyciflorus females responded to the current sex ratio indirectly by adjusting the production of mictic offspring. The response to the population sex ratio allows B. calyciflorus individuals to use indirect cues to perceive the density of males and females separately, providing a fine-scale plastic adjustment in sexual reproduction, rather than population density only.

With a potentially very short growing season as in some temporary ponds or abrupt risks of extinction (e.g. from predators), a safe strategy is to start sexual reproduction even at very low population densities [39]. Although this may come at the cost of short-term fitness, it enhances the long-term probability of population persistence by ensuring the production of some resting eggs soon after colonization of the pond. In such scenarios, sexual reproduction occurs independent of population density as a bet-hedging strategy, while subsequent sex could be triggered by the male-biased population sex ratio. Sexual reproduction initiation in a rotifer population, even at low initial levels of sex, would promote increased engagement in sex, and reproductive coordination would be improved (e.g. through improved quorum sensing). This nonlinear, runaway mechanism could well prepare populations to cope with highly uncertain environmental conditions.

While the association of sexual reproduction with population density in rotifers is frequently assumed [40,41], our results revealed that the population sex ratio in the mother's environment can affect the extent to which offspring respond to population densities (figures 2 and 4). Repression of mictic female production in a female-biased environment has important consequences for the heterogonic life cycle of rotifers, in which there is a trade-off between female parthenogenesis and sexual reproduction. A low population sex ratio, especially after a bout of sexual reproduction, usually indicates a decrease in future population size. Repression of sexual reproduction could restart the phase of female parthenogenesis and, if environmental conditions permit, increase the population size before the initiation of sexual reproduction. In other scenarios, amictic females hatched from resting eggs (stem females), and those from the next few parthenogenetic generations also have a suppressed sexual reproduction, which is called delayed mixis [25]. A low propensity for mictic female production in early generations from resting eggs in B. calyciflorus may increase fitness by increasing the likelihood that sexual reproduction coincides with high conspecific population densities, which may be particularly important in B. calyciflorus at the clonal-population level [25].

There is growing evidence that the maternal environment, including population density [14,42] and food conditions [43], has potential influence on population dynamics by influencing growth and reproductive parameters of offspring [44]. Our population experiment showed that population sex ratio-induced maternal effect on offspring sexual reproduction could lead to marked differences in population dynamics in the rotifer B. calyciflorus. Population densities decreased and recovered to variable degrees among the three population sex ratio treatments (figure 3). The mean offspring number per mother produced did not differ significantly among the three treatments (electronic supplementary material, figure S4); therefore, we can speculate that the clear differences in population dynamics might have been due to variation in the mixis ratio of the offspring (electronic supplementary material, figure S5). Stelzer [20,21] reported the role of density-dependent sexual reproduction in population regulation in B. calyciflorus: when population density reached a threshold, sex was induced and high rates of sexual reproduction necessarily resulted in lower population growth, which in turn led back to asexuality and population growth. Consistent with Stelzer [20,21], we confirmed the role of sexual reproduction in influencing population dynamics, but we further found that sexual reproduction was also affected by the population sex ratio in the mother's environment.

Populations in the male-biased treatment of our short-term population experiment simulated the ‘early growing season’ conditions, where populations accumulated via parthenogenetic reproduction, and the populations were about to start sexual reproduction. Accordingly, population sizes were positively related to the future abundance of mictic females, and initiating sexual reproduction during this period would increase diapausing egg production. Our female-biased treatment simulated periods when RMFs were relatively common. In this low population sex ratio period, most females in the population did not contribute to current population growth. Reducing sexual investment would be adaptive for two reasons. First, the intrinsic costs of sexual reproduction (e.g. at the cost of amictic female production) outweighed the benefits of resting egg production. Second, it allowed continued population growth via female parthenogenesis after a period of sexual reproduction and adaptively prepared amictic offspring for population recovery when the environmental conditions were still suitable for population growth, thus saving the population from collapsing due to excessive sexual reproduction. The ultimate cause for variations in population dynamics remains differences in investment in sex, but our results revealed how the population sex ratio in the mother's environment affected offspring sexual reproduction and finally played a role in population regulation.

The mechanism underlying how mothers detect and respond differently to densities of male-producing and RMFs is unknown. In Daphnia, females are larger than males, which possibly allows individual perception of the sex ratio. However, in rotifers, the MMFs and RMFs do not differ in body size. The density-dependent or quorum-sensing mechanism responsible for the induction of mictic females in Brachionus is due to the accumulation of an info-chemical released into the environment by the rotifers themselves [45]. It is also possible that info-chemicals could be sex-specific, as in copepods [46], enabling more precise estimation of the presence and abundance of different types of conspecies. A mating behaviour in B. calyciflorus might support this prediction—males prefer younger mictic females over older females, because only in these young females can mictic eggs be fertilized and develop into resting eggs [47].

5. Conclusion

In this study, we demonstrated that population sex ratio in the mother's environment altered offspring sexual reproduction, and thus brought population-level consequences. Instead of traditional extrinsic or intrinsic immediate regulating factors, our study emphasized the role of maternal effects in regulating population dynamics. Specifically, we show that population sex ratio in the mother's environment should be considered in the prediction of future population dynamics.

Data accessibility

The raw data are supplied as electronic supplementary material [48].

Authors' contributions

W.L.: conceptualization, data curation, formal analysis, investigation, methodology, resources, software and writing—original draft; C.N.: conceptualization, data curation, funding acquisition, project administration, supervision and writing—review and editing; S.B.: data curation. All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Competing interests

The authors have no conflicts of interest to declare.

Funding

This work was supported by the National Natural Science Foundation of China (grant nos. 32071528 and 31470445).