Mating Delay Reduces Reproductive Performance but Not Longevity in a Monandrous Moth

Journal of Insect Science, (2020) 20(2): 3; 1–5 doi: 10.1093/jisesa/ieaa009 Research

Mating Delay Reduces Reproductive Performance but not Longevity in a Monandrous Moth

Xia-Lin Zheng,1 Junyan Liu,1,2 Wen Lu,1,3 Xiong Zhao He,2 and Qiao Wang2

1Guangxi Key Laboratory of Agric-Environment and Agric-Products Safety, National Demonstration Center for Experimental Plant Science Education, College of Agriculture, Guangxi University, Nanning 530004, China, 2School of Agriculture and Environment, Massey University, Private Bag 11222, Palmerston North, New Zealand, and 3Corresponding author, e-mail: [email protected]

Subject Editor: Oliver Martin

Received 5 December 2019; Editorial decision 10 February 2020

Abstract Age at mating is one of the most important factors that affect mating success and reproductive fitness in insects. The present study investigated how the age of the two sexes at mating determined mating success, reproductive fitness and longevity in Phauda flammans (Walker) (Lepidoptera: Phaudidae), a serious pest of Ficus spp. trees in South and Southeast Asia. The study may provide basic knowledge for the development of mating disruption programs using sex pheromones to control this pest. The species is monandrous and its adults live for only 4–5 d. We show that delayed mating significantly lowered mating success in both sexes, with males being more severely affected than females. Mating delay also reduced reproductive outputs of both sexes but females were more negatively affected than males. We did not find any effect of delayed mating on longevity of either sex. Our findings suggest that mating disruption with sex pheromones can be an effective method to delay mating in P. flammans, reducing reproductive success and thus limit population growth.

Key words: delayed mating, mating success, reproductive output, mating disruption

Age is an important factor that can affect mating success in insects 2018). Various authors suggest that in response to delayed mating, (e.g., Amoah et al. 2019, Lai et al. 2020). Depending on the status adults invest more in somatic maintenance for future reproduc- of mates in an arena, either sex can be choosy. For example, males tion (Proshold et al. 1982, Fadamiro and Baker 1999, Burke and should be choosy when they contribute considerable investment to Bonduriansky 2018) or mating opportunities (Milonoff 1995, Wu the offspring (Bonduriansky 2001, Edward and Chapman 2011, Ng et al. 2018). However, mating delay can also reduce adult longevity et al. 2017, Kaufmann and Otti 2018) while in many cases males (Leather et al. 1985, Bakker et al. 2011, Ricciardi et al. 2019). For compete for access to females and females tend to be choosy (Kokko example, females experiencing delayed mating could allocate their et al. 2003, Puurtinen and Fromhage 2017, Kelly 2018, Li and resources to eggs immediately after fertilization, reducing their Holman 2018). overall longevity (Bakker et al. 2011, De Loof 2011). Age at mating is one of the most important elements influencing Phauda flammans (Walker) (Lepidoptera: Phaudidae) is a mate preference and fitness outcome in insects (e.g., Jiménez-Pérez serious pest of Ficus spp. trees in China (Liu et al. 2016), India and Wang 2003, Xu and Wang 2009, Martin et al. 2016, Kelly 2018, (Nageshchandra et al. 1972, Verma and Dogra 1982), Vietnam (Fof Lai et al. 2020). However, age-dependent mating success and fitness 2015), and Thailand (Anonymous 2018). Its biology (Liu et al. 2014, consequences appear to be divergent in different species. For ex- 2015a, 2015b, 2016; Zheng et al. 2017) and management (Zheng ample, in some species, females may prefer older males for mating et al. 2015, 2019; Huang et al. 2019) are well investigated, making to gain higher genetic quality for their offspring (Simmons 1995, De it a suitable model for the study of age-dependent mating success Luca 2015). In other species, females are more likely to mate with and fitness consequences. Phauda flammans is a monandrous moth younger males to benefit from the higher breeding value and fewer and its adults live for 4–5 d (Liu 2018). Most moths could mate deleterious mutations (Beck and Powell 2000, Beck and Promislow within the first or second day after emergence with mating peak be- 2007). Previous studies show that males may prefer younger females tween the ninth and tenth hours of the photophase (Zheng et al. to produce more progeny (Polak et al. 1998, Nandy et al. 2012, 2019). So far, nothing is known about how the age of the two sexes Mphosi 2019) or older females to gain greater fecundity and fertility at mating affects mating success, reproductive fitness and longevity (Wang et al. 2016, Lentini et al. 2018). in this species, knowledge of which will be of significance for the Recent studies demonstrate that delayed mating may increase understanding of its mating system and development of its pest man- adult longevity (Mori and Evenden 2013, Yang et al. 2017, Wu et al. agement programs such as mating disruption. For example, mating

© The Author(s) 2020. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), 1 which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 Journal of Insect Science, 2020, Vol. 20, No. 2 delays caused by mating disruption may reduce mating success, re- egg hatch (%) = a × male age + b × female age + c × male age × fe- productive output and thus plant damage. male age, where a, b and c are the regression coefficients (i.e., slopes). Based on the information outlined above, we postulate that in Only significant parameters were included in the final model. Data P. flammans 1) younger males and females achieve higher mating on adult longevity were not normally distributed even after trans- success; 2) mating delay of either sex reduces reproductive output; formation, and thus analyzed using a nonparametric analysis of vari- and 3) delayed mating increases longevity of both sexes. To test these ance (ANOVA; GLM Procedure) followed by Bonferroni (Dunn) t hypotheses, we carried out mating trials with nine age combinations Tests for multiple comparisons. A level of P < 0.05 was accepted as of the two sexes and recorded mating success, the number of eggs statistically significant. laid and fertilized, and adult longevity. Results Materials and Methods Effect of Adult Age on Mating Success Insects Mating success significantly decreased with the increase of male Mature P. flammans larvae were collected on Ficus concinna age (F = 10.99, df = 1, 5, P = 0.021) (Fig. 1). Although female age (Miq.) Miq. and F. benjamina L. at Guangxi University (108°29′E, alone did not affect mating success significantly (F = 6.12, df = 1, 22°85′N), Nanning, China, in late June 2016. We reared them in 50 4, P = 0.069), male and female age had significant interactions on transparent plastic containers (15 × 10 × 8 cm), each with 20–30 mating success and with the increase of age in both sexes, mating pinholes (≈1 mm in diameter). We kept 30 larvae in each container success significantly decreased (F = 206.13; df = 1, 5; P < 0.001) with fresh F. concinna leaves as food. The leaves were replaced with (Fig. 1). fresh ones and the number of larvae counted once a day until pu- pation. Dead larvae, if any, were replaced with live ones. The pupae Effect of Adult Age at Mating on Reproductive were sexed according to Mao et al. (2017) and kept individually in Fitness and Longevity plastic tubes (2.7 × 10.3 cm) with a plastic lid bearing 10–15 pin- Age of both sexes at mating significantly negatively affected fecundity holes (≈1 mm in diameter) to obtain virgin adults of different ages. (F = 21.77, df = 1, 145, P < 0.001 for female; F = 11.66 df = 1, 145; Adults were given 10% sucrose solution (Liu et al. 2015b). The in- P < 0.001 for male; Fig. 2A) and egg hatch rate (F = 17.91, df = 1, sects were maintained and all experiments carried out at 26 ± 2°C, 145; P < 0.001 for female; F = 9.12, df = 1, 145, P = 0.003 for male; 70 ± 10% relative humidity, and a photoperiod of 16: 8 (L:D) h. Fig. 2B). However, adult age at mating had no effect on female (mean ± SE, 4.82 ± 0.29 d; range, 4.00–5.26 d) and male longevity Effect of Adult Age on Mating Success (mean ± SE, 3.66 ± 0.21 d; range, 3.41–4.00 d) (F = 1.94, df = 8, Because adult moths normally live for about 4 d (Liu 2018), we set 139, P = 0.059 for female; F = 0.62, df = 8, 139, P = 0.758 for male). up nine combinations of pairing (treatments): 3 female ages (1, 2, and 3 d old) × 3 male ages (1, 2 and 3 d old). Virgin moths of different ages were randomly selected and paired individually in a gauze cage Discussion (50 cm length × 50 cm width × 180 cm height) until death. Thirty The present study demonstrates that the age at mating nega- replicates were performed for each treatment. Observation on each tively affected reproductive performance in the monandrous moth treatment started immediately after moths were paired using four P. flammans but the extent of the impact differed between the sexes. digital video cameras (DS-2CD3T45D-13, Hikvision, Co., Ltd., We reveal that aging in males or both sexes reduced mating success Hangzhou, China). Pairs that mated successfully in each treatment significantly (Fig. 1). This suggests that senescence has more negative were recorded to calculate the mating success rate (number of mated influence on male mating success and females are choosier in terms pairs / total number of observed pairs × 100%).

Effect of Moth Age at Mating on Reproductive Performance and Longevity We provided fresh F. concinna branches with leaves in each of the above 30 cages as oviposition substrates, which were replaced daily. The number of eggs laid on the leaves of branches by each mated female was counted daily under a stereomicroscope (M205C, Leica, Germany). All eggs (<24 h old) laid by each mated female were intro- duced into a transparent plastic Petri dish (10 cm in diameter) for hatching. They were checked three times (0600, 1400, and 2200 hours) a day and hatch rate (the number of hatched larvae / total number of eggs laid × 100%) was recorded. The longevity of both sexes was recorded.

Statistical Analysis Data analysis was performed using SAS software (SAS Institute 2011). Normality of data was tested prior to analysis using a Shapiro–Wilk test (UNIVARIATE Procedure). Data on mating success, fecundity and egg hatch rate affected by female age and male Fig. 1. Effect of female and male age on mating success in P. flammans. age were normally distributed and thus analyzed using a linear re- Mating success (%) = 60.00 + 10.31 × male age—2.78 × male age2 – 3.21 × male gression model (GLM Procedure): mating success (%), fecundity or age × female age (F = 146.68; df = 3, 5; P < 0.001; R2 = 0.989). Journal of Insect Science, 2020, Vol. 20, No. 2 3

less courtship (Moore and Moore 2001). With variable age of both males and females, we indicate that the age of the sexes had significant interactions in mating success and when both sexes were oldest, their mating success reached the minimum (Fig. 1), suggesting that female age also plays a role in mating success when males are older. We show that the age at mating of both sexes significantly reduced fecundity and fertility in P. flammans (Fig. 2), corroborating previous reports on several other insect species (e.g., Kawazu et al. 2014, Yang et al. 2017, Dhillon et al. 2019). Our data do not support the notion that older males are of higher quality (Simmons 1995, De Luca 2015) and older females lay more eggs on average (Wang et al. 2016, Lentini et al. 2018). Similar to S. litura (Wu et al. 2018) and Lasioderma serricorne (F.) (Amoah et al. 2019), the negative impact of aging on reproductive output of P. flammans was more severe in females than in males (Fig. 2), suggesting that eggs are more sensitive than sperm to senescence of their carriers. So far, many studies have demon- strated that mating delay drastically reduces reproductive output of female moths (e.g., Torres-Vila et al. 2002, Mori and Evenden 2013). However, in a seed beetle Acanthoscelides obtectus (Say) (Maklakov et al. 2007), females that mate early in life suffer a significant reduc- tion in lifetime fecundity probably because there are direct costs asso- ciated with mating early in life for females of this species. The effect of mating delay on adult longevity varies in different species. In some species, delayed mating may increase the adult longevity (Mori and Evenden 2013, Yang et al. 2017, Wu et al. 2018) to reduce energy expenditure for future reproduction (Proshold et al. 1982, Fadamiro and Baker 1999, Burke and Bonduriansky 2018) or mating opportunities (Milonoff 1995, Wu et al. 2018). Mating delay can also reduce adult longevity in several other species (Leather et al. 1985, Bakker et al. 2011, Ricciardi et al. 2019) probably because delayed mating triggers females to quickly allocate their resources to eggs (Bakker et al. 2011, De Loof 2011) and males to ejaculate (Harwood et al. 2015) immediately after mating, resulting in early death. However, our data demonstrate that, similar to several species (e.g., Maklakov et al. 2007, Jones et al. 2008, Kawazu et al. 2014, Amoah et al. 2019), adult age at mating had no significant effect on female and male longevity in P. flammans. It is thus likely that these species do not experience a trade-off between reproduc- Fig. 2. Effects of female and male age on fecundity and egg hatch (%) in tion and longevity (Moore and Moore 2001). Furthermore, adults P. flammans. (A) fecundity = 123.81 – 5.54 × male age—7.48 × female age (F = 15.79; df = 2, 145; P < 0.001; R2 = 0.179); (B) egg hatch (%) = 97.32 – that live a very short life in monandrous species like P. flammans 2.62 × male age—3.63 × female age (F = 12.78; df = 2, 145; P < 0.001; may not be able to extend (or shorten) their longevity to trade-off R2 = 0.150). for reproduction. Overall, the present study provides the first empirical evidence of mates’ age in this species, probably because eggs are more expen- for the effect of mating delay on reproductive fitness in the monan- sive than sperm (Darwin 1871). Because younger males carry fewer drous pest P. flammans. We show that older males and females have deleterious mutations (Beck and Powell 2000, Beck and Promislow lower mating and reproductive success. Adult age at mating neither 2007), females could also benefit from mating with young mates. increases nor reduces female and male longevity. Our findings sug- Similarly, aging affects males more severely than females in mating gest that mating disruption using female sex pheromones can be an success in a moth Cnephasia jactatana Walker (Jiménez-Pérez and effective method to delay mating in P. flammans, reducing repro- Wang 2003), and females prefer to mate with younger males, re- ductive success and thus suppressing population growth. sulting in lower mating success in older males in another moth Dendrolimus punctatus Walker (Lai et al. 2020). Acknowledgments Previous studies indicate that mating delay in both sexes results We thank two anonymous reviewers for their constructive comments, which in significantly lower mating success in Cnaphalocrocis medinalis have significantly improved the article. The study was supported by theNa - Guenée (Kawazu et al. 2014) and Spodoptera litura (Fabricius) tional Natural Science Foundation of China (31660206) and the Guangxi (Wu et al. 2018). However, similar to Lobesia botrana (Denis and Scholarship Fund of Guangxi Education Department. Schiffermüller) (Torres-Vila et al. 2002) and Planococcus ficus (Signoret) (Lentini et al. 2018), female age alone did not affect References Cited mating success significantly in P. flammans (Fig. 1). This may be because males are less choosy, tending to mate as many females as pos- Amoah, B. A., R. M. Mahroof, A. R. Gerken, and J. F. Campbell. 2019. sible (Bateman 1948), or older females reduce choosiness and require Effect of delayed mating on longevity and reproductive performance of 4 Journal of Insect Science, 2020, Vol. 20, No. 2

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