Can the extremely female-biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?

Ecological Entomology (2007), 32, 597–602 DOI: 10.1111/j.1365-2311.2007.00908.x

© 2007 The AuthorsJournal compilation © 2007 The Royal Entomological Society 597

Introduction

Most animals have 1:1 sex ratios and Fisher (1930) showed that frequency-dependent selection favours genotypes that allocate equal effort to producing sons and daughters. However, some animals show female-biased sex ratios. As an explanation for such female-biased sex ratios, Hamilton (1967) proposed the local mate competition (LMC) model: female-biased sex ratios are favoured in species where a small number of fertilised fe-males found a patch, and their offspring mate only within that patch before the females disperse. Hamilton showed the gener-ality of the LMC model by listing several animals, including mites, as an important group, all of which have female-biased sex ratios and whose life histories are expected to fit to the as-sumptions of his model. Thereafter, the female-biased sex ra-tios observed in mites have been considered evidence for Hamilton’s theory ( Wilson & Colwell, 1981; Charnov, 1982; Wrensch & Ebbert, 1993; Nagelkerke & Sabelis, 1996 ), if there are no other factors that proximately skew the sex ratios, such as the infection of Wolbachia (e.g. O’Neill et al. , 1997; Stouthamer et al. , 1999 ).

Spider mites are phytophagous and haplodiploid, and their sex ratios are generally female biased (e.g. Sabelis, 1991 ). Their lives satisfy the basic assumptions of the LMC model: arrhe-notoky, patchy distribution with low dispersal ability ( Mitchell, 1973 ), existence of strong male-to-male mate competition ( Potter et al. , 1976a ,b; Saito, 1990, 1995 ), and female dispersal after mating ( Mitchell, 1973 ). Therefore, such female-biased sex ratios have long been considered to be a result of LMC ( McEnroe, 1969 ; Charnov, 1982; Roeder, 1992; Roeder et al. , 1996 ), or its revised version, the subdivided haystack model ( Nagelkerke & Sabelis, 1996 ). However, whether spider mite females actually alter the sex ratio of their progeny depending on the number of patch-mates has only been reported in a single species, the two-spotted spider mite, Tetranychus urticae Koch ( Roeder, 1992; Roeder et al. , 1996 ).

It is known that sex ratios vary among spider mite species, and the communally social species Stigmaeopsis longus (Saito) and Stigmaeopsis miscanthi (Saito) both show extremely female-biased sex ratios. When a single female oviposits in the laboratory, the proportion of females is 0.80 – 0.90 ( Saito & Ueno, 1979 ; Y. Sato and Y. Saito, unpublished data). In the field, one to several fertilised females found each new nest and repro-duce within it for a long period ( Saito, 1987 ). Mating occurs inside the nest in all seasons except the winter diapausing pe-riod. Most progeny mate and reproduce within the natal nests, which the mites are continually enlarging, and large groups are

Correspondence: Yukie Sato, National Institute for Agro-Environmental Sciences, 3-1-3, Kannondai, Tsukuba, Ibaraki 305–8604, Japan. E-mail: [email protected]

Can the extremely female-biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?

Y U K I E S AT O a n d Y U TA K A S A I T O Laboratory of Animal Ecology, Department of Ecology and

Systematics, Graduate School of Agriculture, Hokkaido University, Sapporo, Japan

Abstract . 1. Extremely female-biased sex ratios are known in the social spider mite species, Stigmaeopsis longus and S. miscanthi . Whether Hamilton’s local mate com-petition (LMC) theory can explain such sex ratios was investigated.

2. Significant changes of the progeny sex ratios in the direction predicted by the LMC model were found in both species when the foundress number changed. Therefore, LMC can partly explain the skewed sex ratios in these species.

3. When the foundress number increased, the progeny sex ratio was still female biased and significantly different from the prediction of the LMC model for haplodiploidy. Relatedness between foundresses could not fully explain the female-biased sex ratios. Therefore, these results suggest that there are factors other than LMC skewing the sex ratios of these species toward female.

Key words . Acari , female-biased sex ratio , haplodiploidy , local mate competition , social spider mite , Stigmaeopsis longus , Stigmaeopsis miscanthi , Tetranychidae .

598 Yukie Sato and Yutaka Saito

© 2007 The AuthorsJournal compilation © 2007 The Royal Entomological Society, Ecological Entomology, 32, 597–602

gradually formed. Finally, up to three generations sometimes overlap in a nest ( Saito, 1983, 1995, 1997; Saito et al. , 2000 ). Nest members show obvious waste management behaviour ( Saito, 1983, 1995, 1997; Sato et al. , 2003; Sato & Saito, 2006 ) and cooperative defence behaviour against predatory intruders ( Saito, 1986a,b; Mori & Saito, 2004, 2005 ), to maintain the large group for a long period.

As such, the females experience various nest-mate densities during oviposition. Under such circumstances, each female would be expected to control her progeny sex ratio in response to her nest-mate density during oviposition. Whether these mite species can change their progeny sex ratios as their density during ovi-position increases was investigated to understand what kind of models for biased sex ratio are applicable to these mite species.

Materials and methods

Mites

Stigmaeopsis longus was collected from dwarf bamboo ( Sasa senanensis Franch. et Sav.; Gramineae) in Sapporo (Hokkaido Prefecture, Japan) on 18 May 2000, and S. miscanthi was col-lected from perennial grass ( Miscanthus sinensis Anderss; Gramineae) in Tobuko (Nagasaki Prefecture, Japan) on 29 July 1998. After sampling, each species was reared on the detached leaves of its respective host plant under controlled conditions of 23 ± 2 °C, 40 – 70% RH, and LD 15:9 h photoperiod. All experi-ments mentioned hereafter were also conducted under these conditions. Each laboratory culture was initiated from more than 50 females collected arbitrarily in the field.

Detection of Wolbachia infection

In order to check for a proximate factor that sometimes causes skewed sex ratio, the Wolbachia infection status of the mite populations were determined by PCR using Wolbachia 16S rDNA specific primer ( O’Neill et al. , 1992 ). The PCR was a slight modification of the procedure followed by Gomi et al. (1997) . Wolbachia -infected Panonychus mori Yokoyama and ddH 2 O were used for positive and negative controls respectively.

Foundress number

Three different foundress densities were set for each species: one foundress (a single fertilised female oviposits per nest), two foundresses (two fertilised females oviposit per nest), and five foundresses (five fertilised females oviposit per nest). A piece of host leaf (3 × 1 cm) was placed on a water-soaked polyurethane mat in a Petri dish and surrounded with water-soaked cotton. Females were introduced onto the leaf, allowed to construct a single nest and oviposit for 5 days. If the introduced females constructed more than one nest during the experiment, the rep-licate was omitted from the analysis. Sex ratios were calculated by rearing all progeny until adulthood. Fertilised females aged

4 or 5 days after maturity were used as foundresses in the experiment.

Statistical analysis

The effects of foundress density on the progeny sex ratio of each species were assessed using a logistic regression model ( Sokal & Rohlf, 1995 ). To confirm whether there were any ef-fects such as environmental degeneration or density dependence by increased female density, the numbers of eggs per female were analysed using anova. Progeny survival rates were ana-lysed using a logistic regression model. These analyses were conducted using the computer software, jmp (version 5 for Windows, SAS Institute Inc., Cary, NC, U.S.A. ).

The progeny sex ratios were then compared with the LMC model predictions for haplodiploidy, [ ( n – 1 ) ( 2 n – 1 ) ] / [ n ( 4 n – 1 ) ] , in which n is the foundress number ( Hamilton, 1979; Taylor & Bulmer, 1980 ). The predicted values were confirmed as to whether they fell within the 99% confidence limit of the ob-served data after being arcsine-root transformed by the Freeman – Tukey method in order to ensure normality ( Mosteller & Youtz, 1961 ).

Results

Detection of Wolbachia infection

Wolbachia was detected in six (26.1%) out of 23 S. longus females, but was not detected in any of the 22 S. miscanthi fe-males, although a sufficient amount of mite DNA was extracted from these samples.

Foundress number

The numbers of eggs per female were not significantly affected by foundress density in either species ( S. longus : F 2,80 = 1.988, P = 0.1326; S. miscanthi : F 2,72 = 0.107, P = 0.8989; Fig. 1). Likewise, progeny survival rates were not significantly affected by foun-dress density in either species ( S. longus : overall model: � 2

2 = 4 . 422 , P = 0.1096, foundress density: Wald � 2

2 = 3 . 810 , P = 0.149; S. miscanthi : overall model: � 2


2 = 3 . 221 , P = 0.199, Fig. 2). On the other hand, the progeny sex ratios of both species were significantly affected by foundress density ( S. longus : overall model: � 2


2 = 8 . 268 , P = 0.016; S. miscanthi : overall model: � 2


2 = 10 . 604 , P = 0.005; Fig. 3). These results indicate that females of both species change their progeny sex ratios depending upon the number of foundresses in the nest.

When there were two foundresses, the mean progeny sex ratio and the 99% confidence limit of transformed data for S. longus was 0.219 (0.487 radians) and 0.190 – 0.249 (0.451 – 0.523 radians), and 0.475 (0.498 radians) and 0.201 – 0.256 (0.465 – 0.531 radians) for S. miscanthi . The LMC model pre-diction was 0.214 (0.481 radians), within the 99% confidence

LMC in social spider mites 599


limit of the observed progeny sex ratio in both species. On the other hand, when the foundress number was 5, the mean prog-eny sex ratio and the 99% confidence limit of transformed data of S. longus were 0.200 (0.464 radians) and 0.176 – 0.226 (0.433 – 0.495 radians), and 0.248 (0.521 radians) and 0.203 – 0.296 (0.467 – 0.575 radians) for S. miscanthi . The LMC model prediction was 0.379 (0.663 radians), significantly higher than the observed progeny sex ratio in both S. longus and S. miscanthi .

Discussion

LMC

The progeny sex ratios of S. longus and S. miscanthi moved significantly in the direction predicted by the LMC model when the foundress number per nest changed (Fig. 3). Because there is no significant difference in immature survival rate be-tween different foundress densities in either species (Fig. 2), the present results clearly indicate that the LMC model is applicable to the female-biased sex ratios observed in both species. However, a part of the sex-ratio bias in these spider mites remains unexplained. If LMC is the only factor underlying the biased sex ratio, 0.379 is predicted at five foundresses per nest, while 0.200 was observed in S. longus and 0.248 was observed in S. miscanthi . Therefore, there is 13 – 18% female excess (called surplus female-biased sex ratio hereafter) in the experimental data of both species. Other

potential factors must be considered in order to explain their surplus female-biased sex ratios.

Wolbachia infection

Reproductive modification by micro-organisms, for example Wolbachia , an alpha proteobacteria infecting a wide range of arthropods, is known to cause cytoplasmic incompatibility, par-thenogenesis, feminisation, and male-killing (e.g. O’Neill et al. , 1997; Stouthamer et al. , 1999 ). Wolbachia has been detected in spider mites, and several studies have reported sex ratio alterna-tion ( Breeuwer, 1997; Vala et al. , 2000, 2003a,b ; Gotoh et al. , 2003, 2005 ). Although most of these reported male-biased sex ratio as cytoplasmic incompatibility, Vala et al. (2000 , 2003a) reported that infected females produced significantly more female-biased sex ratios than uninfected (cured) females in T. urticae .

In the present study, several Wolbachia- infected S. longus fe-males were found, but all the S. miscanthi females were unin-fected, whereas a surplus ratio was observed in both species. Furthermore, the 26.1% S. longus infection rate observed in the present study is insufficient to explain the female-biased sex ra-tio in S. longus . Even if a Wolbachia infection renders a female capable of producing only daughters and the rest of the females produce progeny in the way of the LMC model prediction without consideration of nest-mate’s Wolbachia infection, the expected mean progeny sex ratio becomes 0.28 per nest when foundress number is 5. This expected value is still more male-biased

Fig. 1. Numbers of eggs per female at three different foundress densities in Stigmaeopsis longus and S. miscanthi .

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Fig. 2. Progeny survival rates at three dif-ferent foundress densities in Stigmaeopsis longus and S. miscanthi .



than the 99% confidence limit of data from the present study (0.176 – 0.226) for S. longus , which requires an infection proportion of at least 40.4% to be consistent. The present results may not always be sufficient to completely negate the effects of micro-organisms on the sex ratios of these mite species, because there is no way to guarantee the non-existence of such organ-isms by PCR. However, they must decrease the probability that the sex ratios of these mites are caused by such proximate factors.

Male aggression theory

The parasitoid wasp, Melittobia australica (Eulophidae), is known to show a more extreme female-biased sex ratio than predicted by the usual LMC and inbreeding models ( Abe et al. , 2003b ). Abe et al. (2003b) proposed a new idea that a mother should save her male progeny if there is fatal competition be-tween males, and two studies by Abe et al. (2003a, 2005) sup-port and reinforce this idea. In S. miscanthi , male-to-male competition is extremely high ( Saito, 1995 ), and the female-biased sex ratio in this species fits well with their theory. However, there is no male-to-male competition in S. longus ( Saito, 1990 ), even though the sex ratio is skewed to almost the same extent as in highly aggressive S. miscanthi . Therefore, male-to-male com-petition theory cannot explain the present case.

Foundress relatedness

The extent of the optimal sex allocation bias resulting from LMC is predicted to vary according to the relatedness among offspring ( Frank, 1986, 1987 ). Tetranychus urticae can manipu-late sex ratio in response to the relatedness of patch mates in the direction predicted by sex allocation theory ( Roeder et al. , 1996 ). It is thought that the life types and life schedules of S. longus and S. miscanthi will occasionally lead to higher relat-edness among nest mates ( Saito, 1987, 1995, 1997 ), and such high relatedness seems to explain the surplus female-biased sex ratio in S. longus and S. miscanthi .

The extent of inbreeding in both species using mean progeny sex ratios and the LMC model equation for haplodiploidy can be estimated as r = [ ( n – 1 ) ( 2 – h ) ] / [ n ( 4 – h ) ] , where r (0 < r < 1) is the observed progeny sex ratio, n is the foundress number, and h (0 < h <1) is the amount of inbreeding ( Frank, 1985; Herre,

1985; Werren, 1987 ). If n = 5 and r = 0.296 (the largest value of 99% confidence limit of S. miscanthi ), we obtain h = 0.825 from h = [ 2 n ( 1 – 2 r ) – 2 ] / [ n ( 1 – r ) – 1 ] . Thus the observed value can be realised if S. miscanthi is under extremely high inbreeding conditions. However, if n = 5 and r = 0.226 (the largest value of 99% confidence limit of S. longus ), the amount of inbreeding, h , is 1.213, indicating that the observed S. longus sex ratio is more greatly skewed to female than predicted by the LMC with inbreeding model. Anyhow, from the above calcula-tion there remains a possibility that the overall sex ratios ob-served in both S. miscanthi and S. longus can be explained by LMC with inbreeding only if they are under extreme inbreeding conditions.

Population structure

The LMC prediction used in this paper is based on the island model where the population has a simple group structure and each group lasts only one generation. However, Stigmaeopsis mite populations have a more complicated structure because of their short generation times, long oviposition times, and low ability to disperse, which make each group last several genera-tions. The population structure influences both within- and between-group selection. Therefore, the influence of population structure must be considered in relation to LMC and the related-ness between foundresses. Nagelkerke and Sabelis (1996) de-veloped the haystack model by subdividing each group into one-generation mating groups, in which each group lasts several generations. This model succeeded in explaining the surplus female-biased sex ratio in mites and some small arthropods. Because there is no detailed population structure data for S. longus or S. miscanthi , there is no way to simulate the optimal sex ratios in the subdivided haystack model. However, their model may be very useful in explaining the surplus female-biased sex ratios in these mites, as already suggested by Nagelkerke and Sabelis (1996) .

Acknowledgements

I thank Drs E. Hasegawa, T. Mitsunaga, S. Miyai, K. Mori, T. Sakagami, Y. Suzuki, and Y. Watanuki for their valuable sugges-tions and help. I also appreciate the efforts of Dr A. R. Chittenden who kindly reviewed the manuscript. This work was supported

Fig. 3. Progeny sex ratios (male ratio) at three different foundress densities in Stigmaeopsis longus and S. miscanthi .

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LMC in social spider mites 601


by Research Fellowships for Young Scientists and Grant-in-Aid for scientific Research (KAKENHI: B-17370005) from the Japan Society for the Promotion of Science, and by MEXT through Special Co-ordination Funds for Promoting Science and Technology.

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Accepted 19 February 2007First published online 1 October 2007

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Can the extremely female-biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?