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Older mothers produce smaller eggs without compromising offspring quality: a study of a thelytokous mite predator (Acari: Phytoseiidae)

Published online by Cambridge University Press:  18 November 2024

Keshi Zhang Open the ORCID record for Keshi Zhang [Opens in a new window] ,
Zhenguo Liu Open the ORCID record for Zhenguo Liu [Opens in a new window]  and
Zhi-Qiang Zhang Open the ORCID record for Zhi-Qiang Zhang [Opens in a new window]
Keshi Zhang
Affiliation:
School of Biological Sciences, University of Auckland, Auckland 1072, New Zealand Manaaki Whenua – Landcare Research, Auckland 1072, New Zealand
Zhenguo Liu
Affiliation:
Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Shandong Provincial Key Laboratory of Animal Nutrition and Efficient Feeding, Department of Animal Science, Shandong Agricultural University, Taian, Shandong 271017, People's Republic of China
Zhi-Qiang Zhang*
Affiliation:
School of Biological Sciences, University of Auckland, Auckland 1072, New Zealand Manaaki Whenua – Landcare Research, Auckland 1072, New Zealand
*
Corresponding author: Zhi-Qiang Zhang; Email: [email protected]
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Abstract

Negative relationships between the parental age and offspring life history traits have been widely observed across diverse animal taxa. However, there is a lack of studies examining the influence of parental age on offspring performance using mites, particularly phytoseiid predators as subjects. This study explored the influence of maternal age on offspring life history traits in Amblyseius herbicolus (Chant) (Acari: Mesostigmata), a phytoseiid predatory mite reproducing through thelytokous parthenogenesis. We hypothesised that increased maternal age negatively impacts offspring traits, including developmental duration, body size, fecundity and lifespan. Amblyseius herbicolus was reared under controlled laboratory conditions, and the life history traits of offspring from mothers of varying ages were analysed using linear mixed-effect models. Our results showed that the increase in maternal age significantly reduced individual egg volume, but did not significantly affect offspring developmental duration, body size, fecundity or lifespan. These findings indicate that while older A. herbicolus females produced smaller eggs, the subsequent performance (i.e. body size, fecundity and lifespan) of offspring remained largely unaffected, suggesting possible compensatory mechanisms in the offspring or alternative maternal provisioning strategies. The results of this study offer useful insights into the reproductive strategies of phytoseiid predators and asexually reproducing species, enhancing our understanding of how maternal age affects offspring fitness. Further studies can examine how offspring of A. herbicolus from mothers of different ages perform under adverse environmental conditions.

Keywords

ageingAmblyseius herbicolusLansing effectmaternal ageparental influenceparthenogenesis
Type
Research Paper
Information
Bulletin of Entomological Research , First View , pp. 1 - 8
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This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
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Copyright © The Author(s), 2024. Published by Cambridge University Press

Introduction

Ageing is a fundamental characteristic of most living organisms (Harman, Reference Harman2001; López-Otín et al., Reference López-Otín, Blasco, Partridge, Serrano and Kroemer2013; Dodig et al., Reference Dodig, Čepelak and Pavić2019). The process of ageing involves the accumulation of structural damage, such as deleterious cellular and tissue changes, leading to functional decline, increased mortality risk and reduced reproductive potential (Harman, Reference Harman2001; Weinert and Timiras, Reference Weinert and Timiras2003; López-Otín et al., Reference López-Otín, Blasco, Partridge, Serrano and Kroemer2013; Flatt and Partridge, Reference Flatt and Partridge2018; Lemoine, Reference Lemoine2020). While ageing is essential for evolutionary processes (Harman, Reference Harman2001; López-Otín et al., Reference López-Otín, Blasco, Partridge, Serrano and Kroemer2013), its role and mechanisms in natural selection remain a complex puzzle for researchers (Lemoine, Reference Lemoine2020). Although numerous hypotheses have been proposed to explain the causes and controls of ageing, defining and proving these mechanisms remains challenging (Harman, Reference Harman2001; López-Otín et al., Reference López-Otín, Blasco, Partridge, Serrano and Kroemer2013). Both intrinsic and extrinsic factors, including development, genetic defects, environmental influences and disease, contribute to the complex interactions of ageing (Takahashi et al., Reference Takahashi, Kuro-O and Ishikawa2000; Harman, Reference Harman2001; Dodig et al., Reference Dodig, Čepelak and Pavić2019; Lemoine, Reference Lemoine2020).

Ageing affects not only an individual but also has intergenerational effects on its offspring (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020). For instance, the negative relationship between the parental age and offspring lifespan, known as the ‘Lansing effect’, has been widely observed across diverse animal taxa, particularly in iteroparous species (species with multiple reproductive cycles during their lifetime) (Lansing, Reference Lansing1947; Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020). A meta-analysis indicates a general tendency for invertebrates, such as insect species and rotifers, to exhibit the Lansing effect more than mammals and birds (Ivimey-Cook et al., Reference Ivimey-Cook, Shorr and Moorad2023). Further studies indicate that parental age at reproduction not only influences offspring lifespan but also affects other fitness-related traits, such as fecundity, leading to potential long-term consequences (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020; Noguera, Reference Noguera2021; Dupont et al., Reference Dupont, Barbraud, Chastel, Delord, Pallud, Parenteau, Weimerskirch and Angelier2023). For example, the offspring of old red flour beetle (Tribolium castaneum) parents had a reduced tolerance to starvation compared to those of young parents (Halle et al., Reference Halle, Nowizki and Scharf2015). The mechanisms underlying these parental age-related effects remain elusive but may include gamete quality deterioration, reduced parental investment (e.g. post-hatching parental care), and increased inbreeding chances and associated costs (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020).

Mites (Acari) are ideal for ageing studies due to their small size, short lifespan and ease of obtaining large numbers (Boczek and Czajkowska, Reference Boczek and Czajkowska1973; Li, Reference Li2019). Previous research has explored factors such as diet, predator stress, social environment and mating frequency on mite lifespan (e.g. Gotoh and Tsuchiya, Reference Gotoh and Tsuchiya2008; Li and Zhang, Reference Li and Zhang2018, Reference Li and Zhang2019, Reference Li and Zhang2021; Wei and Zhang, Reference Wei and Zhang2022). However, limited studies have examined the influence of parental age on offspring performance in mites. Offspring of older parents in the flour mite (Acarus siro) exhibit reduced fecundity in females and lifespan in males (Boczek and Czajkowska, Reference Boczek and Czajkowska1973) with age; similarly, offspring of older soil mites (Sancassania berlesei) exhibit reduced lifespan and egg hatchability, and prolonged immature development (Benton et al., Reference Benton, Clair and Plaistow2008) compared with offspring of younger parents. Additionally, increased parental age is associated with reduced mating success, duration and fertility (Prokop et al., Reference Prokop, Stuglik, Żabińska and Radwan2007; Morita et al., Reference Morita, Ullah, Sugawara and Gotoh2021). For instance, older males of the bulb mite (Rhizoglyphus robini) have reduced mating success, and females mated with older males have lower fecundity than those mated with younger males (Prokop et al., Reference Prokop, Stuglik, Żabińska and Radwan2007).

The family Phytoseiidae (Acari: Mesostigmata) contains predominantly free-living predators, many of which are crucial biocontrol agents against agricultural pests (Zhang, Reference Zhang2003). Species such as Amblyseius swirskii, Neoseiulus cucumeris and Phytoseiulus persimilis are widely used biocontrol agents (Amano and Chant, Reference Amano and Chant1977; Zhang, Reference Zhang2003; McMurtry et al., Reference McMurtry, Moraes and Sourassou2013). Amblyseius herbicolus (Chant) (Acari: Mesostigmata) is a generalist predatory mite with the potential for controlling thrips, psyllids, whiteflies and various pest mites (Reis et al., Reference Reis, Teodoro, Neto and da Silva2007; Cavalcante et al., Reference Cavalcante, Santos, Rossi and de Moraes2015; Kalile et al., Reference Kalile, Cardoso, Pallini, Fonseca, Elliot, Fialho, Carvalho and Janssen2021; Lam et al., Reference Lam, Paynter and Zhang2021; Xin and Zhang, Reference Xin and Zhang2021). Unlike most sexually reproducing phytoseiid species (Hoy, Reference Hoy1985; Norton et al., Reference Norton, Kethley, Johnston, O'Connor, Wrensch and Ebbert1993), A. herbicolus reproduces asexually via thelytokous parthenogenesis, with no observed males (Zhang and Zhang, Reference Zhang and Zhang2022).

Understanding the effects of parental age on reproduction sheds light on broader fields such as life history evolution, reproductive scheduling, parental investment and conservation medicine (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020). Our system, using A. herbicolus provides a unique opportunity to examine maternal effects without paternal influences, genetic recombination or post-hatching parental care, which minimises confounding factors. Additionally, A. herbicolus demonstrates distinct life history strategies by producing fewer but larger eggs compared to other previously studied mite species, such as A. siro, R. robini and S. berlesei, in the context of maternal age influence on offspring (Benton et al., Reference Benton, Lapsley and Beckerman2001; Plaistow et al., Reference Plaistow, Clair, Grant and Benton2007; Sánchez-Ramos and Castañera, Reference Sánchez-Ramos and Castañera2007; Puspitarini et al., Reference Puspitarini, Fernando, Widjayanti, Purwanti, Munthe, Aini and Wildaniyah2021). Amblyseius herbicolus mothers produce relatively large eggs (about 20% of body size) over multiple weeks, with an oviposition period lasting about 70% of their lifespan and at a rate of averaging one egg per day (Reis et al., Reference Reis, Teodoro, Neto and da Silva2007; Cavalcante et al., Reference Cavalcante, Santos, Rossi and de Moraes2015; Zhang and Zhang, Reference Zhang and Zhang2021). Therefore, we investigated the age-specific influence of mothers at oviposition on offspring life history traits in A. herbicolus. We hypothesised that the increased maternal age could have a negative impact on their offspring's life history traits – including developmental time, body size, fecundity and lifespan. The results of this study can provide valuable insights into the population dynamics of A. herbicolus and other phytoseiid predators, as well as asexually reproducing species that use similar life history strategies.

Materials and methods

Mite rearing and feeding conditions

Adult females (>30 individuals) of A. herbicolus were collected from naturally infested black nightshade (Solanum nigrum L.) (Solanales: Solanaceae) leaves at Manaaki Whenua – Landcare Research, St Johns, Auckland, to establish the initial culture. The A. herbicolus cultures were maintained under laboratory conditions and fed ad libitum on dried fruit mite Carpoglyphus lactis (L.) (Acari: Carpoglyphidae) for approximately 1 year before the experiment. The prey, C. lactis, was obtained from Bioforce Limited (Karaka, Auckland). All cultures and experimental units were maintained in acrylic cabinets at 25 ± 1°C, 80 ± 5% relative humidity and a 16:8 (light: dark) photoperiod.

The culture set-up included a Petri dish containing a mixture of wheat bran, dry yeast and sugar, which was placed on a layer of plastic sheet to feed C. lactis (see Wang et al., Reference Wang, Zhang, Li and Zhang2024 for details). The plastic sheet was positioned on top of a sponge to prevent flooding. This sponge was centrally placed in a plastic container filled with water to confine both mite species.

Rearing cells

We used enclosed cells for the individual rearing of A. herbicolus, with slight modifications to the size of the arena compared to those used in Zhang and Zhang (Reference Zhang and Zhang2021). Each experimental cell consisted of two plexiglass slides. The top slide had a cone-shaped hole (top diameter 6 mm, bottom diameter 3 mm; volume 32.99 mm3) in the centre to accommodate mites. This hole was covered with a piece of food wrap on the top and with black plastic film underneath to enhance visibility. To facilitate air and moisture exchange, small holes were made in both the wrap and the plastic film using an insect pin (size 0). Additionally, filter papers placed beneath the plastic film provided a water source for the mites. The bottom plexiglass slide, along with two foldback clips, was used to assemble the cell securely.

Experimental procedures

Offspring (eggs) of A. herbicolus were obtained from another study (Liu et al., Reference Liu, Zhang and Zhang2024a). In Liu et al. (Reference Liu, Zhang and Zhang2024a), mothers of A. herbicolus were provided with a total of 40 frozen eggs of C. lactis during immature development, and five frozen adult females of C. lactis replenished daily during adulthood. Eggs of C. lactis were collected using the method described in Liu et al. (Reference Liu, Zhang and Zhang2024b) and frozen at −18°C for about a month before the experiment. Filtered water (c. 2 μl) was provided daily to A. herbicolus using a pipette from the larval stage. Five mothers were excluded from the study; two did not lay eggs, and three were lost during feeding. A total of 336 eggs from 14 mothers were obtained and examined in this study (table 1).

Table 1. Reproductive parameters of Amblyseius herbicolus mothers fed with 40 frozen eggs of Carpoglyphus lactis during immature development and five frozen adult females of C. lactis replenished daily during adulthood

Mean ± SEM (maximum–minimum) of ovipositional duration and fecundity are summarised.

All collected eggs were measured under an interference phase-contrast microscope (SMZ25, Nikon Corporation, Japan) at 200× magnification before being individually reared using modified Munger cells. The size of individual eggs was measured by their volume, calculated using the formula in Narushin (Reference Narushin2005). The individual egg volume (V) was determined using the length (L) and maximum breadth (B) of the eggs:

$$V = ( 0 .6057 - {\rm \;0}{\rm .0018B) }LB^ 2$$

The eggs collected from A. herbicolus (i.e. those from Liu et al., Reference Liu, Zhang and Zhang2024a) were reared individually in modified Munger cells with ad libitum live mixed-stage C. lactis to examine the influence of maternal age at oviposition on the life history traits of offspring. Sufficient dry yeast pellets were added to each cell to feed C. lactis and replenished as needed. Water was supplied daily by moistening the filter papers in the cells. These individually reared A. herbicolus were observed daily (at midday) to examine developmental duration (from egg to adult), fecundity (total lifetime oviposition), pre-oviposition period (number of days from adulthood to first oviposition), oviposition period (duration from the first to last day of oviposition), post-oviposition period (time from the last oviposition to death), daily oviposition rate (average number of eggs laid per day) and lifespan (from egg to death). At death, adult A. herbicolus females were slide-mounted in Hoyer's medium and oven-dried at 40°C for a week (Walter and Krantz, Reference Walter, Krantz, Krantz and Walter2009). The size of individuals at maturity was determined by measuring the dorsal shield length at 200× magnification using an interference phase-contrast microscope. The dorsal shields of adult phytoseiid species, including A. herbicolus, are sclerotised and, like other arthropod species, show minimal changes after reaching maturity (Zhang, Reference Zhang2003; Hanna et al., Reference Hanna, Lamouret, Poças, Mirth, Moczek, Nijhout and Abouheif2023; Ma et al., Reference Ma, Zhang, Fan and Zhang2024). Thus, the length of the dorsal shield measured in this study represents their size at maturity.

The slides were vouchered in the New Zealand Arthropod Collection (NZAC), Auckland, New Zealand, and Shanghai Natural History Museum (SNHM), Shanghai, China.

Statistical analysis

R (R Core Team, 2022) was used for statistical analysis. The packages ggplot2 (Wickham, Reference Wickham2016) and lme4 (Bates et al., Reference Bates, Mächler, Bolker and Walker2015) were used to generate graphs and perform linear modelling, respectively. Linear mixed-effect models were used to determine the influence of maternal age at oviposition on egg size (individual egg volume), and maternal age and egg size on the life history traits (developmental duration, body size, fecundity, pre-ovipositional duration, ovipositional duration, post-ovipositional duration, daily oviposition and lifespan) of the offspring. Wald χ2 tests were used to assess the significance of individual predictors. Since the eggs were obtained from different mothers, the individual mothers were used as a random factor in the linear mixed-effect models. The random factor had no significant influence on the models examined in this study. Equations of the regression lines (line of best fit) were given in figures. Pearson's correlations were also performed to determine the relationship between two variables. Statistical significance was set at P < 0.05.

Results

Influence of maternal age at oviposition on offspring size

The maternal age at oviposition of A. herbicolus significantly affected the volume of individual eggs (linear mixed-effects model: Wald χ2 = 49.784, df = 1, P < 0.001). Specifically, egg volume decreased with increasing maternal age (fig. 1).

Figure 1. Relationship between individual egg volume of Amblyseius herbicolus offspring and maternal age at oviposition. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equation is shown on the graph. Pearson's correlation: t = −7.071, df = 334; the P-value is shown on the graph.

Performance of offspring

Neither the maternal age at oviposition (linear mixed-effects model: Wald χ2 = 3.068, df = 1, P = 0.080) nor individual egg volume (Wald χ2 = 3.232, df = 1, P = 0.072) significantly influenced the body size at maturity of A. herbicolus offspring (fig. 2A, B). Additionally, the interaction between these two parameters did not significantly affect offspring body size (Wald χ2 = 0.402, df = 1, P = 0.526). The maternal age at oviposition did not significantly affect offspring developmental duration (Wald χ2 = 0.313, df = 1, P = 0.576). However, larger eggs had a significantly shorter developmental duration compared to smaller eggs (Wald χ2 = 4.332, df = 1, P = 0.038) (fig. 2D). The interaction between the individual egg volume and maternal age at oviposition was also significant (Wald χ2 = 5.745, df = 1, P = 0.017), with the maternal age indirectly influencing developmental duration (fig. 2C) through its effect on egg volume (fig. 1), and with egg volume significantly affecting developmental duration (fig. 2D).

Figure 2. Body size (measured by the dorsal plate length) and developmental duration (from egg to adult) of Amblyseius herbicolus offspring vs. maternal age at oviposition and initial egg size (volume) of offspring. (A) Body size vs. age at oviposition; (B) body size vs. egg volume; (C) developmental duration vs. age at oviposition; (D) developmental duration vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = 1.436; (B) t = 1.492; (C) t = 0.690; and (D) t = −2.371; P-values are shown on the graphs.

The maternal age at oviposition (linear mixed-effects model: Wald χ2 = 0.031, df = 1, P = 0.860) and initial egg size (Wald χ2 = 1.153, df = 1, P = 0.283) did not significantly affect the fecundity of A. herbicolus offspring. However, a significant interaction between maternal age at oviposition and initial egg size was observed in relation to offspring fecundity (Wald χ2 = 1.552, df = 1, P = 0.213), reflecting an inverse relationship between these factors. Despite the significant interaction, the relationships between maternal age and initial egg size with offspring fecundity were not significant (fig. 3A, B). Similarly, maternal age at oviposition (Wald χ2 = 0.171, df = 1, P = 0.679) and initial egg size (Wald χ2 = 0.130, df = 1, P = 0.719) did not significantly affect the lifespan of offspring, nor were there significant relationships between these factors and offspring lifespan (Wald χ2 = 1.153, df = 1, P = 0.283) (fig. 3C, D).

Figure 3. Fecundity and lifespan of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Fecundity vs. age at oviposition; (B) fecundity vs. egg volume; (C) lifespan vs. age at oviposition; (D) lifespan vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 146 for all correlations; (A) t = −0.095; (B) t = 0.590; (C) t = −0.209; and (D) t = −0.128; P-values are shown on the graphs.

The maternal age at oviposition and initial egg size had no significant effects on the pre-oviposition period (linear mixed-effects model: Wald χ2 = 0.655, df = 1, P = 0.418 for maternal age at oviposition; Wald χ2 = 2.242, df = 1, P = 0.134 for initial egg size), oviposition period (Wald χ2 = 2.903, df = 1, P = 0.088 for maternal age at oviposition; Wald χ2 = 0.782, df = 1, P = 0.376 for initial egg size) or post-oviposition period (Wald χ2 = 3.326, df = 1, P = 0.068 for maternal age at oviposition; Wald χ2 = 0.041, df = 1, P = 0.839 for initial egg size) of A. herbicolus offspring (figs 4 and 5). Additionally, no significant interaction was found between these two factors (i.e. maternal age at oviposition and initial egg size), except for the oviposition period (Wald χ2 = 7.089, df = 1, P = 0.008). While maternal age at oviposition and initial egg size had opposite effects on the oviposition period, neither was statistically significant (fig. 5A, B). However, the daily oviposition rate of offspring was significantly influenced by the maternal age at oviposition (Wald χ2 = 15.721, df = 1, P < 0.001), but not by initial egg size (Wald χ2 = 0.133, df = 1, P = 0.715), and no significant interaction between the factors was observed (Wald χ2 = 0.070, df = 1, P = 0.792). Specifically, offspring of older mothers exhibited a higher daily oviposition rate compared to those of younger mothers (fig. 5C).

Figure 4. Pre-oviposition period and post-oviposition period of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Pre-oviposition period vs. age at oviposition; (B) pre-oviposition period vs. egg volume; (C) post-oviposition period vs. age at oviposition; (D) post-oviposition period vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = 0.542; (B) t = 1.378; (C) t = −1.812; and (D) t = 0.134; P-values are shown on the graphs.

Figure 5. Oviposition period and daily oviposition rate of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Oviposition period vs. age at oviposition; (B) oviposition period vs. egg volume; (C) daily oviposition rate vs. age at oviposition; (D) daily oviposition rate vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = −1.867; (B) t = 1.200; (C) t = 3.993; and (D) t = −0.356; P-values are shown on the graphs.

Discussion

This study examined the effect of maternal age on offspring life history traits in the thelytokous phytoseiid predator A. herbicolus. The results revealed a significant trend: as the maternal age at oviposition increased, A. herbicolus females produced smaller eggs. This finding is consistent with the general pattern observed in many arthropod species, such as the bruchid seed beetle (Callosobruchus maculatus), where advancing maternal age is typically associated with a reduction in egg size (Fox, Reference Fox1993; Fox and Czesak, Reference Fox and Czesak2000). The influence of maternal age on egg size is probably due to a depletion of females' resources (Fox, Reference Fox1993). The survival cost of reproduction has also been proposed as a critical factor influencing the relationship between egg size and maternal age, with a reduction in egg size associated with increased survival of mothers without a significant decrease in their fecundity (i.e. offspring quantity) (see Kindsvater et al., Reference Kindsvater, Bonsall and Alonzo2011). Previous studies using phytoseiid species, including P. persimilis (Toyoshima and Amano, Reference Toyoshima and Amano1998; Han et al., Reference Han, Zhang, Chen and Zhang2024) and N. cucumeris (Lee et al., Reference Lee, Fan and Zhang2020) have found that egg size correlates with maternal dietary condition, whereby individuals with better feeding produce larger eggs than those with poorer feeding. However, the diet given to A. herbicolus mothers in this study was replenished daily without any changes in quantity. Therefore, it remains to be investigated whether an age-related reduction in physiological functions, such as metabolism, or a shift in resource allocation between somatic maintenance and reproduction affected the offspring size of A. herbicolus.

Contrary to our expectations, maternal age in A. herbicolus did not significantly influence offspring developmental duration, body size, reproductive parameters or lifespan, indicating an absence of the Lansing effect in these traits. The influence of aged parents on offspring performance is not always negative (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020). For instance, older parents may produce longer-lived offspring when they have access to more food or an increase in experience. Individuals may also increase reproductive effort if their life expectancy is short, a phenomenon known as ‘terminal investment’ (Monaghan et al., Reference Monaghan, Maklakov and Metcalfe2020). As noted earlier, phytoseiid species such as A. herbicolus produce relatively large eggs, averaging about one egg per day during oviposition (Zhang and Zhang, Reference Zhang and Zhang2021; table 1). Especially towards the end of their oviposition, A. herbicolus females can take up to 4 days before laying one egg (Zhang K, personal observation). Therefore, A. herbicolus mothers probably maintained their offspring or gamete quality even with a reduction in egg size. Moreover, the significant increase in daily oviposition rate observed in offspring of older mothers, compared to those of younger mothers, suggests that these offspring are not disadvantaged by maternal ageing, at least under optimal food conditions. However, further studies are necessary to validate these findings.

The absence of a negative relationship between egg size and subsequent performance in body size, lifespan and reproductive parameters in A. herbicolus could be attributed to the provision of abundant feed, preventing dietary stress or restriction throughout their life course. Larger offspring of taxonomically diverse animal species often exhibit better survival in adverse environmental conditions compared to smaller ones (Fischer et al., Reference Fischer, Taborsky and Kokko2011). For instance, a study on the seed-feeding beetle Stator limbatus suggests that egg size does not affect the performance of subsequently hatched offspring without stress or poor conditions (Fox and Mousseau, Reference Fox and Mousseau1996).

The variability in egg size relative to maternal age is complex and context dependent. It is influenced by numerous environmental factors (Plaistow and Benton, Reference Plaistow and Benton2009; Rollinson and Hutchings, Reference Rollinson and Hutchings2013; van Daalen et al., Reference van Daalen, Hernández, Caswell, Neubert and Gribble2022). For instance, the parasitic wasp Eupelmus vuilleti showed no difference in egg size, but older females produced eggs containing less protein, sugar and lipids than younger females (Muller et al., Reference Muller, Giron, Desouhant, Rey, Casas, Lefrique and Visser2017). Whether A. herbicolus mothers can reduce the size of their offspring without reducing the essential nutrients for development requires further investigation.

We found that the A. herbicolus that hatched from larger eggs had a significantly shorter developmental duration than those from smaller eggs. The significant interaction between individual egg volume and maternal age observed in this study suggests that while maternal age alone may not directly influence offspring traits, its combined effect with egg size can impact offspring developmental duration. The egg size correlates with the initial offspring resource and size, which can significantly affect offspring fitness, especially for species without parental care (Fox et al., Reference Fox, Czesak, Mousseau and Roff1999; Dias and Marshall, Reference Dias and Marshall2010; Marshall et al., Reference Marshall, Heppell, Munch and Warner2010). For example, larger eggs were associated with faster immature development in other arthropod species, such as the seed beetle C. maculatus (Fox, Reference Fox1994). Although larger eggs may confer developmental advantages (Fox et al., Reference Fox, Czesak, Mousseau and Roff1999; Bonduriansky, Reference Bonduriansky and Pfennig2021), in our study the initial egg size of A. herbicolus did not influence offspring body size, fecundity or lifespan, which suggests that later feeding could compensate for the poor start (smaller initial egg size).

One limitation of this study was that the mothers were not given ad libitum feed (i.e. those from Liu et al., Reference Liu, Zhang and Zhang2024a). Since all prey given was consumed, especially during adulthood, A. herbicolus mothers were probably facing dietary restrictions and used different reproductive strategies during the experiment. Caloric restriction has been found to compensate for the adverse influence of the Lansing effect in the monogonont rotifer Brachionus manjavacas (Gribble et al., Reference Gribble, Jarvis, Bock and Welch2014). Furthermore, the extent of increase in egg mass as mothers age in Hippodamia convergens has been found to be modulated by their diet as immatures and by their size at maturity (Vargas et al., Reference Vargas, Michaud and Nechols2012). Therefore, further studies could investigate the influence of maternal age on offspring in A. herbicolus by eliminating the influence of dietary restriction. Moreover, daily observations may be insufficient to capture subtle variations in developmental durations of these rapidly developing predators. Increasing the frequency of monitoring could be beneficial for detecting finer differences in future studies.

Despite the absence of Lansing effect in A. herbicolus, maternal age at oviposition affected the egg size, which then affected the offspring developmental time. Thus, maternal age may have an alternative route in shaping the life history strategies of this species. These results highlight the complex interactions between maternal age and offspring traits and provide insights into the reproductive strategies of asexually reproducing species like A. herbicolus. Further research is needed to explore the underlying mechanisms and the potential influence of varying environmental conditions on these maternal effects.

Acknowledgements

We thank Helen O'Leary of Manaaki Whenua – Landcare Research for her constructive comments and suggestions that improved this manuscript. We thank Bioforce Limited for providing the initial population of C. lactis. This study was supported in part by New Zealand Government core funding for Crown Research Institutes from the Ministry of Business, Innovation, and Employment's Science and Innovation Group. Zhenguo Liu was supported by the Chinese Scholarship Council and Research Funds of Shandong Agricultural University, PRC.

Competing interests

None.

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Figure 0

Table 1. Reproductive parameters of Amblyseius herbicolus mothers fed with 40 frozen eggs of Carpoglyphus lactis during immature development and five frozen adult females of C. lactis replenished daily during adulthood

Figure 1

Figure 1. Relationship between individual egg volume of Amblyseius herbicolus offspring and maternal age at oviposition. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equation is shown on the graph. Pearson's correlation: t = −7.071, df = 334; the P-value is shown on the graph.

Figure 2

Figure 2. Body size (measured by the dorsal plate length) and developmental duration (from egg to adult) of Amblyseius herbicolus offspring vs. maternal age at oviposition and initial egg size (volume) of offspring. (A) Body size vs. age at oviposition; (B) body size vs. egg volume; (C) developmental duration vs. age at oviposition; (D) developmental duration vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = 1.436; (B) t = 1.492; (C) t = 0.690; and (D) t = −2.371; P-values are shown on the graphs.

Figure 3

Figure 3. Fecundity and lifespan of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Fecundity vs. age at oviposition; (B) fecundity vs. egg volume; (C) lifespan vs. age at oviposition; (D) lifespan vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 146 for all correlations; (A) t = −0.095; (B) t = 0.590; (C) t = −0.209; and (D) t = −0.128; P-values are shown on the graphs.

Figure 4

Figure 4. Pre-oviposition period and post-oviposition period of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Pre-oviposition period vs. age at oviposition; (B) pre-oviposition period vs. egg volume; (C) post-oviposition period vs. age at oviposition; (D) post-oviposition period vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = 0.542; (B) t = 1.378; (C) t = −1.812; and (D) t = 0.134; P-values are shown on the graphs.

Figure 5

Figure 5. Oviposition period and daily oviposition rate of Amblyseius herbicolus offspring regressed against maternal age at oviposition and initial egg size (volume) of offspring. (A) Oviposition period vs. age at oviposition; (B) oviposition period vs. egg volume; (C) daily oviposition rate vs. age at oviposition; (D) daily oviposition rate vs. egg volume. The regression line (black) is accompanied by the 95% confidence interval (grey margins). The regression equations are shown on the graphs. Pearson's correlation: df = 135 for all correlations; (A) t = −1.867; (B) t = 1.200; (C) t = 3.993; and (D) t = −0.356; P-values are shown on the graphs.