Introduction
The Tetranychid mite Panonychus ulmi Koch (Acari Tetranychidae), commonly named European red spider mite, is one of the most economically important plant-feeding mites reported on various crops around the world (Rode et al., Reference Rode, Ferla, Bizarro, Schussler and Ferla2024b, Reference Rode, Schneider, Mariano, Matthes and Ferla2024a). Panonychus ulmi is a mite that primarily infests apple trees, although it has also been documented on 171 different host plants across various plant families (Migeon and Dorkeld Reference Migeon and Dorkeld2025). Both P. ulmi immatures and adults consume the cellular contents of leaves, compromising photosynthetic function and reducing the percentage of essential mineral elements, such as nitrogen, phosphorus, and potassium (Cao et al., Reference Cao, Sun, Shao, Wang, Zhu, Long, Geng and Zhang2025; Mirsoleimani et al., Reference Mirsoleimani, Najafi-Ghiri, Heydari and Farokhzadeh2021).
Improving knowledge of the population dynamics of mite and insect pests is crucial for accurately predicting outbreaks, which are primarily linked to the overuse of non-selective pesticide treatments, leading to the development of resistance and the loss of natural enemies (Li and Yang Reference Li and Yang2015). In view of this phenomenon, earlier studies investigating pyrethroid resistance in related mite species, such as Tetranychus urticae Koch (Acari: Tetranychidae), have indicated that this resistance is associated with point mutations in the gene that codes for the voltage-gated sodium channel. In contrast, glutamate-gated chloride channels (GluCls) are recognised target sites for abamectin, and it has been demonstrated that changes in amino acids within GluCls can lead to resistance against abamectin (Rameshgar et al., Reference Rameshgar, Khajehali, Nauen, Bajda, Jonckheere, Dermauw and Van Leeuwen2019b, Reference Rameshgar, Khajehali, Nauen, Dermauw and Van Leeuwen2019a).
Panonychus ulmi is capable of producing offspring through both bisexual reproduction and arrhenotokous parthenogenesis (Normark and Kirkendall Reference Normark, Kirkendall, Resh and Cardé2009). Arrhenotoky exemplifies a unique mode of parthenogenesis in which unfertilised eggs develop into males, whereas fertilised eggs give rise to females (Sperling and Glover Reference Sperling and Glover2023; Subramanian et al., Reference Subramanian, Boopathi, Sagar and Omkar2022). It contrasts with thelytoky, a form of reproduction in which females produce only daughters without requiring mating (Mozhaitseva et al., Reference Mozhaitseva, Tourrain and Branca2023). Arrhenotokous reproduction is common in mite groups, such as Mesostigmata, Prostigmata, and Astigmata, which directly affects their reproductive rates and overall population structure (Häußermann et al., Reference Häußermann, Giacobino, Munz, Ziegelmann, Palacio and Rosenkranz2020; Liu et al., Reference Liu, Wu, Liang, Zhou and Huang2022). When present, arrhenotoky serves as the primary reproductive mechanism among many closely related species within specific genera, subfamilies, or families (Ding et al., Reference Ding, Chi, Gökçe, Gao and Zhang2018). This reproductive mechanism holds considerable importance for population expansion, as it enables virgin females to sustain their lineage by producing male progeny, who subsequently contribute to the development of a bisexual cohort through oedipal mating (McCulloch and Owen Reference McCulloch and Owen2012).
Numerous life tables and population parameters of P. ulmi have been studied based on female age-specific life table analysis, which do not clarify the contribution of arrhenotokous reproduction to population growth (Gotoh et al., Reference Gotoh, Ishikawa and Kitashima2003; Herbert Reference Herbert1981; Johann et al., Reference Johann, Do Nascimento, da Silva, da Silva Carvalho and Juarez Ferla2019). However, these conventional life tables fail to account for the male population and its impact on the sex ratio, and also inadequately depict stage differentiation. In this study, we examine the effects of both reproductive strategies and construct separate life tables for P. ulmi cohorts exhibiting bisexual and arrhenotokous reproduction through the age-stage, two-sex life table model (Chi Reference Chi1988; Chi and Liu Reference Chi and Liu1985). This model addresses the challenges of variability in individual development and stage differentiation. Life table data were then used for population projections to determine potential differences in population growth and management arising from the two strategies.
Materials and methods
Origin, identification, and rearing of mites
Panonychus ulmi specimens were collected from apple leaves of the Jeromine cultivar, which is grown in the Arbor orchard located in the Oulmes region of Morocco (33°25'46.03”N, 5°59'14.10”W). The P. ulmi identification was confirmed based on visual examination of morphological features (Razuvaeva et al., Reference Razuvaeva, Ulyanova, Skolotneva and Andreeva2023). Apple leaves with mites were preserved in 70% ethanol. Microscopic preparations were made employing modified Faure–Berlese medium, with Hoyer’s medium (Walter and Krantz Reference Walter, Krantz, Krantz and Walter2009). Mite species were identified by L. Allam under transmitted light using a phase-contrast microscope at magnifications ranging from 10 to 1000 times, with the literature sources (Kamayev et al., Reference Kamayev, Anorbayev and Obidjanov2024; Kreiter et al., Reference Kreiter, Auger, Grissa, Tixier, Chermiti and Dali2003; Naves et al., Reference Naves, Nóbrega and Auger2021).
Spider mites were reared on twenty potted green bean plants, Phaseolus vulgaris L. (Fabales: Fabaceae), according to the technique proposed by Bustos et al. (Reference Bustos, Rodríguez, Cure and Cantor2016). This method takes into consideration both plant growth and P. ulmi population dynamics. The young green bean plants, potted in 2 L pots containing rice husk and soil (1:2), were initially infested on day 14 with 5 mated P. ulmi females per leaf. For each plant, three entirely developed leaves were selected and isolated using a commercial glue (Vermifix) at the base of the petiole to prevent the mites from escaping. Panonychus ulmi colonies were maintained at 26 ± 1 °C, 65 ± 5% relative humidity (RH), and a 16:8 (L:D) hour photoperiod for two generations before the start of the experiments.
Bisexual life table of P. ulmi
Eighty-three eggs of P. ulmi, all one day old, were collected from rearing units to start the life table study. Each egg was carefully transferred individually with a fine brush onto green bean leaf discs placed on saturated wet cotton inside 9 cm diameter Petri dishes. The development stage and survival data were recorded daily. After the emergence of adults, male and female mites were paired into fifty-five couples for reproduction. Once an individual died during the experiment, an individual of the same sex was isolated from the rearing colony and introduced for reproduction. All drowned or escaped mites recruited were excluded from the life table data analysis. Leaf discs underwent daily inspections, and any stressed leaves were substituted with fresh ones. Lifespan and fecundity were monitored until the death of individuals. Eggs that were newly hatched were transferred individually onto leaf discs, and the offspring were observed until they matured to determine their sex ratio, which was performed based on morphological features (Razuvaeva et al., Reference Razuvaeva, Ulyanova, Skolotneva and Andreeva2023).
Arrhenotokous life table of P. ulmi
Following the emergence of the adult specimens, the virgin females were isolated in individual rearing containers, and the parameters regarding fecundity and survival were meticulously recorded daily. The Arrhenotokous life table of P. ulmi began with a cohort of 58 virgin females. Each newly laid egg was meticulously transferred to an individual leaf disc and monitored daily until the attainment of the adult stage. The first male to emerge was subsequently paired with its mother for mating. Survival rates and daily fecundity were systematically recorded until the death of the maternal subject. If a male died, a new one was selected from the same female’s offspring and replaced. Data for escaped or drowned individuals were excluded from the life table analysis. Eggs produced by mated females were kept separately and reared to adulthood to determine the sex ratio.
Projection
Life table data of both bisexual and arrhenotokous populations of P. ulmi were used to project the population growth over 60 days by using the program TIMING (Chi Reference Chi2025a). With an initial population of 10 P. ulmi eggs, the two-sex life table was used to simulate the growth of the bisexual cohort. In the same way, 10 eggs obtained from oedipal mating were also used to project the arrhenotokous group. The simulation was run with an economic threshold value of 10 % of occupation by one or more mobile forms of P. ulmi per leaf (English-Loeb and Hesler Reference English-Loeb and Hesler2004).
Statistical analysis
Life table and population parameters, including the age-stage specific survival rate Sx,j, age-stage specific fecundity fx,j, age-stage specific life expectancy Ex,j, age-specific survival rate lx, age-specific fecundity rate mx, intrinsic rate of increase r, finite rate of increase λ, the net rate of reproduction R0, and the mean generation time T, were performed using the TWOSEX-MSChart computer program (Chi Reference Chi2025b).
Variances and standard errors were determined using the bootstrap resampling technique with 100,000 resamples (Efron and Tibshirani Reference Efron and Tibshirani1994). The paired bootstrap test evaluated the difference between treatments based on the 95% percentile confidence interval and t-interval of the 100,000 differences (Smucker et al., Reference Smucker, Allan and Carterette2007). All graphs were created using Microsoft Excel 2019 software (Microsoft Corporation 2019).
Results
Development
The developmental duration for bisexual and arrhenotokous populations of P. ulmi is shown in table 1. The results indicate significant differences between individuals of both reproductive groups from the egg to adult stages (P < 0.05). Within the bisexual population, marked differences were identified in the developmental duration of the surviving individuals, specifically between males and females, during both the immature and adult stages (P = 0.0231 and P < 0.05, respectively). Moreover, the developmental duration of females within the bisexual cohort during both the pre-adult and adult stages was significantly prolonged compared to that of the arrhenotokous cohort (P < 0.05). Overall, the development of P. ulmi individuals within the arrhenotokous cohort appears to occur at a faster rate compared to that of the bisexual population.
Table 1. Mean (±SE) of the stage-specific developmental time of Panonychus ulmi bisexual and arrhenotokous cohorts
n: cohort size (bisexual cohort, arrhenotokous cohort).
Means followed by the same small letter within columns and the same capital letter within rows are not significantly different according to the paired bootstrap test (α = 0.05).
SE: standard error.
DBM: difference bootstrap mean.
* P < 0.05, **P < 0.01, ***P < 0.001.
Reproduction
The oviposition parameters for P. ulmi females, which include oviposition days, the adult pre-oviposition period (APOP), the total pre-oviposition period (TPOP), and the effective oviposition (total fecundity), are presented in table 2. In the bisexual cohort, the duration of the oviposition period for females designated to produce female offspring was significantly longer than for those assigned to produce males (P < 0.05). Additionally, the oviposition days for females producing female offspring within the bisexual cohort were significantly longer than those observed in the arrhenotokous cohort (P < 0.05). Conversely, a similar number of oviposition days was recorded for females producing male offspring in both reproductive groups (P = 0.1560) (fig 2).
Table 2. Mean (± SE) of oviposition parameters and fecundity rate of Panonychus ulmi bisexual and arrhenotokous cohorts
n: cohort size (bisexual cohort, arrhenotokous cohort).
Means followed by the same small letter within columns and the same capital letter within rows are not significantly different according to the paired bootstrap test (α = 0.05).
SE: standard error.
DBM: difference bootstrap mean.
* P < 0.05, **P < 0.01, ***P < 0.001.
The duration of APOP needed for the production of female offspring was significantly shorter (P < 0.0001) in bisexual reproduction compared to that observed in P. ulmi arrhenotokous reproduction. Furthermore, the APOP and TPOP required for producing male offspring in arrhenotokous reproduction were significantly shorter than those observed in bisexual reproduction. In contrast, the APOP and TPOP for producing female offspring were deliberately longer in the arrhenotokous group than those associated with bisexual reproduction (P < 0.05). Indeed, there was no difference in the TPOP in producing female and male offspring in bisexual individuals (P = 0.4063) (table 2).
In bisexual reproduction, females produced an average of 47.38 female eggs and 17.38 male eggs throughout their lifespan, whereas arrhenotokous females yielded 8.90 female offspring and 50.21 male offspring (table 2). Although virgin female adults produce only male eggs before oedipal mating, they are capable of generating a greater number of male eggs than bisexual females. Following oedipal mating, the proportion of male eggs declined with the age of the females; the fecundity rate of mated females increased, resulting in the production of a larger quantity of female eggs.
On the other hand, when only female eggs were included in the calculation of population parameters, the values of R0, r, λ, and T were 47.38 offspring, 0.1857 d−1, 1.2041 d−1, and 20.76 days, respectively. In the arrhenotokous group, when all eggs were included in the calculation, these values were 49.17 offspring, 0.2150 d−1, 1.2398 d−1, and 18.11 days, respectively. The values of R0, r, and λ were significantly higher than those found in the bisexual cohort (P < 0.05), while the mean generation time T was shorter than that of the bisexual cohort (P < 0.05). In reality, following the occurrence of arrhenotokous parthenogenetic reproduction within insect and mite populations, calculating population parameters based on the total number of eggs or only female eggs can lead to potentially inaccurate scenarios.
The age-stage specific survival rates of bisexual and arrhenotokous cohorts of P. ulmi are plotted in fig 1. The curves clearly illustrated the overlap among successive life stages from eggs to adults, thereby demonstrating the variable development exhibited by P. ulmi individuals of both reproductive categories. In the bisexual cohort, there were two separate curves for both sexes of P. ulmi adults (fig. 1A), but only a single female adult curve in arrhenotokous reproduction (fig. 1B). The age-stage survival rates of P. ulmi bisexual population were S6,2 = 0.86, S9,3 = 0.77, S11,4 = 0.62 for larvae, protonymphs, and deutonymphs, respectively, while 0.66 and 0.26 for female and male adults occurred respectively at age 17 and 15 days. In the arrhenotokous group, the Sx,j was S5,2 = 0.93 for larvae, S8,3 = 0.86 for protonymphs, S10,4 = 0.62 for deutonymphs, and S13,5 = 0.82 for females.
Figure 1. The age-stage specific survival rate Sx,j of Panonychus ulmi (A) Bisexual reproduction and (B) Arrhenotokous reproduction
Figure 2. Age-specific survival rate (lx), fecundity (mx), and net maternity (lxmx) of bisexual (A) and arrhenotokous (B) Panonychus ulmi
Figure 3 shows the age-stage life expectancies of the bisexual and arrhenotokous cohorts of P. ulmi. This parameter can be used to predict individuals’ future survival time and assist in evaluating the extent and duration of individual damage pests. The result revealed that life expectancies at different ages of the bisexual cohort are mostly higher than those in the arrhenotokous cohort. At age zero E0,1, the life expectancy of P. ulmi bisexual and arrhenotokous cohorts was 30.36 and 26.86 days, respectively, which are consistent with the total longevity (table 1).
Figure 3. The age-stage life expectancy (Ex,j) of Panonychus ulmi (A) Bisexual reproduction; and (B) Arrhenotokous reproduction.
Projection of population
The projected population growth of P. ulmi with bisexual and arrhenotokous reproduction is illustrated in fig 4. The results indicate that the bisexual cohort demonstrates more rapid growth compared to the arrhenotokous cohort. Starting with an initial bisexual population of 10 newborn eggs, the total counts of eggs, larvae, protonymphs, deutonymphs, and both female and male adults after 60 days were 159, 90, 70, 52, 56, and 39, respectively, culminating in a population size of 197 individuals. In the case of arrhenotokous reproduction, the number of individuals originating from 10 eggs of oedipal mated females amounted to 16 eggs, 6 larvae, 6 protonymphs, 6 deutonymphs, and 16 female adults, resulting in a total population of 23 P. ulmi individuals.
Figure 4. Projection of the population growth of P. ulmi from an initial population of 10 Panonychus ulmi newborn eggs without any control. (A) Bisexual group. (B) Arrhenotokous reproduction started with virgin females. Stage size of both bisexual and arrhenotokous cohorts with necessary controls is shown in (C) and (D), respectively. The population and weighted sixes, as well as the cumulative weighted insect days regarding the set economic threshold, are displayed in (E) for bisexual reproduction and in (F) for arrhenotokous reproduction. The black arrows indicate the time of controls.
Assuming a control treatment results in 90% mortality across all stages and the economic threshold is 10 mites per leaf, the bisexual cohort would need a total of three separate treatments on days 20, 37, and 56 to keep the P. ulmi population below the established economic threshold. To maintain the arrhenotokous cohort at the same economic threshold, the first treatment should occur later on day 26, and only one supplementary action is needed on day 47.
The weighted population size and cumulative weighted insect-days (CWID) provide useful information for estimating the weighted effect of the insect population to the crop (or predator to pest) by taking the different consumption rates into account. Nonetheless, the CWID after 60 days of projected growth of P. ulmi without any controls was recorded at 231 individuals for the bisexual cohort, in contrast to 44 individuals for the arrhenotokous group. Upon implementing the scheduled control measures, the CWID was determined to be 19 individuals over the 60-day projection period, regardless of the reproductive circumstances type.
Discussion
This study clarifies and compares the demographic traits of the P. ulmi population, which displays two reproductive modes: bisexual and arrhenotokous, using age-stage, two-sex life table analysis. This analysis accurately fits the life table and population parameters with the required confidence (Chi et al., Reference Chi, Kavousi, Gharekhani, Atlihan, Salih Özgökçe, Güncan, Gökçe, Smith, Benelli, Guedes, Amir-Maafi, Shirazi, Taghizadeh, Maroufpoor, Xu, Zheng, Ye, Chen, You, Fu, Li, Shi, Hu, Zheng, Luo, Yuan, Zang, Chen, Tuan, Lin, Wang, Gotoh, Shaef Ullah, Botto-Mahan, De Bona, Bussaman, Gabre, Saska, Schneider, Ullah and Desneux2023), because the method overcomes the problem associated with applying female age-specific life tables to insect and mite populations (Huang and Chi Reference Huang and Chi2012). The use of traditional life tables to analyse arrhenotokous parthenogenesis does not provide an accurate assessment of the demographic parameters for a target population of insects or mites. This is because virgin females produce only male offspring before they mate, leading to a significant delay in stabilising the age-stage structure of the population (Chen et al., Reference Chen, Luo, Wang, Sun, Wang, Zhou, Luo, Liu, Yan and Wang2025; Chi et al., Reference Chi, Fu and You2019).
In this study, P. ulmi females were able to produce more males through arrhenotoky (table 2), ensuring that mating opportunities remain available even when males are scarce. This flexibility helps maintain genetic diversity and reproductive efficiency (Duan et al., Reference Duan, Li, Zhu, Li, Sun and Wang2016; Ferla et al., Reference Ferla, Granich and Ferla2024). The ability to produce males without mating is widely observed within mite and insect populations, which adapt more quickly to changing environments (Normark and Kirkendall Reference Normark, Kirkendall, Resh and Cardé2009; Weerawansha Reference Weerawansha2023).
When all P. ulmi offspring produced by the arrhenotokous population were included in the calculation, the values of R0, r, and λ were found to be 49.17 offspring, 0.215 d−1, and 1.239 d−1, respectively. But, when only female eggs were considered, R0, r, and λ were 8.89 offspring, 0.098 d−1, and 1.103 d−1, respectively. Both population parameters are erroneous due to the delay that affects the stabilisation of the age-stage structure of the P. ulmi population. Using the age-stage, two-sex life table analysis, the population parameters of the bisexual cohort of P. ulmi were found to be r = 0.1828 d−1, λ = 1.2006 d−1, R0 = 44.80 offspring, and T = 20.79 days. To detect any possible effect of variability of the offspring sex ratio on population parameters, the age-stage-sex method, commonly known 3D life table (Huang and Chi Reference Huang and Chi2011), was also utilised to calculate the population parameters, which were r = 0.1857 d−1, λ = 1.2041 d−1, R0 = 47.38 offspring, and T = 20.76 days. Afterward, we found no significant differences between the results from both methods (P > 0.05) (table 3), which suggests that the sex ratio remained stable in offspring produced at different ages of the females.
Table 3. Population parameters (mean ± SE) of Panonychus ulmi bisexual population based on two-sex and 3D life table analyses
n: cohort size (bisexual cohort, arrhenotokous cohort).
SE: standard error.
DBM: difference bootstrap means.
Means followed by the same letter are not significantly different according to the paired bootstrap test (α = 0.05).
A comprehensive comparative analysis of arrhenotokous parthenogenesis has independently evolved multiple times within arthropods (van der Kooi et al., Reference van der Kooi, Matthey-Doret and Schwander2017). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a common example used for studying arrhenotoky within the Tetranychidae family (Jakubowska et al., Reference Jakubowska, Dobosz, Zawada and Kowalska2022). Tetranychus urticae is a cosmopolitan pest mite whose rapid developmental rate enables it to produce colonies of thousands of individuals within a short time period. When a solitary virgin female colonizes a new host plant, it is capable of producing male offspring through arrhenotokous parthenogenesis, which yields comparable values of both bisexual and arrhenotokous P. ulmi populations (Tuan et al., Reference Tuan, Lin, Yang, Atlihan, Saska and Chi2016). Similarly, arrhenotokous females of Tetranychus ludeni Zacher (Acari: Tetranychidae) contribute to the rapid expansion of their population and the invasion of new habitats (Zhou et al., Reference Zhou, He, Chen and Wang2021). The northern fowl mite Ornithonyssus sylviarum (Acari: Macronyssidae) can establish on new hosts without males present (McCulloch and Owen Reference McCulloch and Owen2012).
While the dominant and ancestral mode of sex determination in Tetranychid mites is arrhenotokous parthenogenesis, the genetic mechanism making arrhenotokous reproduction possible has been confirmed for 4 of 21 hymenopteran superfamilies (Heimpel and de Boer Reference Heimpel and de Boer2008). However, some other hymenopterans from the genus Nasonia (Hymenoptera: Chalcidoidea: Pteromalidae), like Nasonia vitripennis Walker, Nasonia longicornis Werren, Nasonia giraulti Werren, and Nasonia oneida Kevin, do not involve the gene mediating the complementary sex determination (CSD), exhibiting thelytoky or pseudo-arrhenotoky, commonly known as paternal genome elimination (Raychoudhury et al., Reference Raychoudhury, Desjardins, Buellesbach, Loehlin, Grillenberger, Beukeboom, Schmitt and Werren2010), which is often observed across Phytoseiid species (Zhang et al., Reference Zhang, Chen, Wang, Zhang, Wei, Yu, Zheng, Chen, Zhang, Lin, Sun, Liu, Tang, Lei, Li and Liu2019). Phytoseiid mites, such as Amblyseius womersleyi Schicha, Typhlodromus occidentalis Nesbitt, Neoseiulus cucumeris Oudemans, and Phytoseiulus persimilis Athias-Henriot demonstrate precise control over sex allocation. They can adjust sex ratio depending on the density of conspecific females through pseudo-arrhenotokous (Nagelkerke and Sabelis Reference Nagelkerke, Sabelis, Schuster and Murphy1991). Additionally, some species of Thysanoptera, particularly those in the Thripidae family, such as Megalurothrips usitatus Bagnall, Thrips tabaci Lindeman, and Frankliniella intonsa Trybom, are capable of both arrhenotokous and thelytokous reproduction. This demonstrates their evolutionary adaptability in reproductive strategies, allowing for rapid colonisation and population growth in response to specific ecological pressures (Aizawa et al., Reference Aizawa, Watanabe, Kumano, Tamagaki and Sonoda2018; Guo et al., Reference Guo, Wu, Gong and Tang2023; Woldemelak Reference Woldemelak2021).
A primary limitation in our study is the disparity between results obtained under controlled conditions and those observed in the field. However, laboratory experiments are carried out under stable, optimal, and controlled biotic and abiotic factors, whereas field conditions are continuously varying over time (Sarwar Reference Sarwar and Awasthi2020). Variables such as temperature, humidity, photoperiod, soil moisture, pH, and host plant characteristics affect the survival, development, and reproduction rates of pest mites and insects (Martínez-Villar et al., Reference Martínez-Villar, López-Manzanares, Legarrea, Pérez-Moreno and Marco-Mancebón2024; Savi et al., Reference Savi, Gonsaga, de Matos, Braz, de Moraes and de Andrade2021). However, the Sex ratio observed in such populations can also deviate significantly from those determined by laboratory experiments (Liu et al., Reference Liu, Gao, Liu, Guo, Liu, Zhu and Wu2018). This gap highlights a critical need for research methodologies that can effectively study mite reproductive dynamics in the field, accounting for the full spectrum of ecological factors that influence the expression of arrhenotoky in natural populations (Manrakhan et al., Reference Manrakhan, Verykouki, Serfontein, Goldshtein, Beck, Kriticos, Szyniszewska, Kozyra, Papadopoulos and Nestel2025; Tang et al., Reference Tang, Guo, Shen, Chen and Zang2023). For instance, eriophyid mites that reproduce successfully in the lab have been observed to fail under natural field conditions, highlighting the profound impact of environmental and abiotic constraints on population viability (Marini et al., Reference Marini, Weyl, Vidović, Petanović, Littlefield, Simoni, de Lillo, Cristofaro and Smith2021).
Molecular techniques are critical tools for addressing the challenges inherent in mite research (Cruickshank Reference Cruickshank2002). DNA-based methods enable precise species identification and effectively overcome the limitations of traditional morphological analysis, particularly when examining immature specimens (Pereira et al., Reference Pereira, Carneiro and Amorim2008; Tixier et al., Reference Tixier, Dos Santos Vicente, Douin, Duso and Kreiter2017). Population genetics and omic sciences provide valuable tools for conducting a detailed analysis of population structure, gene flow, and dispersal patterns in natural environments, allowing researchers to gain insights without the complexities of tracking individual organisms and yield important perceptions into the evolutionary dynamics of arrhenotoky (Luikart et al., Reference Luikart, Kardos, Hand, Rajora, Aitken, Hohenlohe and Rajora2019; Ragauskas et al., Reference Ragauskas, Maziliauskaitė, Prakas and Butkauskas2025). However, by sequencing the mitochondrial cytochrome oxidase subunit I (COI) gene in 20 species of phytophagous mites from nine genera and two families (Tetranychidae and Tenuipalpidae), including several agricultural pests, it has been shown that there is a trend toward thelytoky becoming less common compared to arrhenotoky, which is the usual mode of reproduction in this group (Navajas et al., Reference Navajas, Gutierrez, Lagnel and Boursot1996).
Overall, the combination of arrhenotoky, high fecundity, and short generation time renders P. ulmi particularly susceptible to rapid population expansion, resulting in pest outbreaks within agricultural environments (Ardeh et al., Reference Ardeh, de Jong and van Lenteren2005; Gokhman and Kuznetsova Reference Gokhman and Kuznetsova2018). On the other hand, while arrhenotoky allows for rapid population growth, it can also lead to reduced genetic diversity over time because males are haploid and inherit only maternal genes (Harper et al., Reference Harper, Bagley, Thompson and Linnen2016; Li and Zhang Reference Li and Zhang2021; Picard et al., Reference Picard, Vicoso, Bertrand and Escriva2021).
Although arrhenotokous parthenogenesis offers several evolutionary advantages, it reduces genetic diversity within populations. This reduction increases vulnerability to environmental changes and disease. Furthermore, the lack of gene recombination in males may limit the ability of populations to adapt to rapidly changing environments or to develop resistance to pesticides (Agut et al., Reference Agut, Pastor, Jaques and Flors2018). Arrhenotoky-driven rapid population growth in P. ulmi complicates management in agricultural fields and greenhouses. This reproductive strategy accelerates the development of pesticide resistance, intensifying pest control challenges.
Acknowledgements
The authors would like to thank Professor Hsin CHI for granting permission to use the analytical tools. They also extend their gratitude to the managers of the Arbor Experimental Station for their assistance with field tasks.
Competing interests
The authors assert that there are no conflicts of interest to disclose.
