J Ethol (2010) 28:483–489 DOI 10.1007/s10164-010-0211-7
ARTICLE
Pairing and insemination patterns in a giant weta (Deinacrida rugosa: Orthoptera; Anostostomatidae) Clint D. Kelly • Luc F. Bussie`re • Darryl T. Gwynne
Received: 14 August 2009 / Accepted: 14 February 2010 / Published online: 8 April 2010 Ó Japan Ethological Society and Springer 2010
Abstract Positive size assortative mating can arise if either one or both sexes prefer bigger mates or if the success of larger males in contests for larger females leaves smaller males to mate with smaller females. Moreover, body size could not only influence pairing patterns before copulation but also the covariance between female size and size of ejaculate (number of spermatophores) transferred to a mate. In this field study, we examine the pre-copulatory mate choice, as well as insemination, patterns in the Cook Strait giant weta (Deinacrida rugosa). D. rugosa is a large orthopteran insect that exhibits strong female-biased sexual dimorphism, with females being nearly twice as heavy as males. Contrary to the general expectation of male preference for large females in insects with female-biased size dimorphism, we found only weak support for positive size assortative mating based on size (tibia length).
C. D. Kelly (&) Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50011, USA e-mail:
[email protected] L. F. Bussie`re School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia L. F. Bussie`re Zoologisches Museum Der Universita¨t Zu¨rich, Zurich, Switzerland D. T. Gwynne Department of Biology, University of Toronto at Mississauga, Mississauga, ON, Canada Present Address: L. F. Bussie`re School of Biological and Environmental Sciences, University of Stirling, Stirling, UK
Interestingly, although there was no correlation between male body size and the number of spermatophores transferred, we did find that males pass more spermatophores to lighter females. This pattern of sperm transfer does not appear to be a consequence of those males that mate heavier females being sperm depleted. Instead, males may provide lighter females with more spermatophores perhaps because these females pose less of a sperm competition risk to mates. Keywords Sexual size dimorphism Assortative mating Sperm competition risk Spermatophore transfer Scramble competition Mate choice
Introduction Sexual competition occurs both prior to mating as well as after if there is competition between rival male ejaculates (Simmons 2001). Such sexual selection often favors large males. Thus, body size does not only play a role in determining the likelihood of pairing or the size of mating partner. For example, precopulatory mate choice that engenders size assortative mating patterns—i.e. the success of larger males in competition for larger females leaves smaller males to mate with smaller females (Crespi 1989)—could also interact with copulatory mate choice to produce intriguing patterns of covariance between the size of mating partners and the outcome of their sexual interaction. In the simplest case, size assortative mating might lead to a positive correlation between female size and ejaculate size because larger males usually have larger testes and therefore larger sperm reserves (e.g., Tomkins and Simmons 2002). However, if larger males are prone to ejaculate depletion because of more frequent mating
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opportunities (Preston et al. 2001; Bussie`re et al. 2005) or engage in strategic ejaculation, either process could mitigate or invert this expected positive covariance (Bussie`re 2002). There is considerable evidence that males often maximize their fitness by strategically allocating sperm to the subset of females providing the greatest fertilization returns (Wedell et al. 2002). As a consequence, larger females may receive even larger ejaculates than expected given the size of their partner because they offer males a fecundity advantage (Reinhold et al. 2002). On the other hand, if larger females tend to mate more often than smaller conspecifics, males may conserve sperm to avoid the greater intensity of sperm competition within the sperm stores of large females, and instead invest more ejaculate in smaller females where the risk or intensity of sperm competition is lower (Wedell et al. 2002). The frequency of these alternative outcomes in natural systems remains unclear, and more work on the interaction between precopulatory and copulatory mating patterns is needed. The Cook Strait giant weta, Deinacrida rugosa (Orthoptera: Anostostomatidae), is a sexually size dimorphic nocturnal insect endemic to New Zealand that is of high conservation importance (Gibbs 2001; McIntyre 2001). This insect inhabits old pastures, forests and coastal scrub, and seeks refuge from predators in the daytime by hiding under vegetation or other objects on the ground (McIntyre 2001). Males do not appear to defend resources required by sexually receptive females nor do they guard harems of females as in other deinacridines (i.e. Hemideina tree weta; McIntyre 2001). Instead, males seek receptive females as mates at night while females are foraging away from refuges (McIntyre 2001). Once a male locates a receptive female, he remains in physical contact with her using either his antennae or legs, and follows her until she finds a diurnal refuge (Richards 1973; McIntyre 2001). The pair will remain together at least until the following night—longer if the weather is cool and wet—copulating repeatedly throughout the day while in the refuge (Richards 1973; McIntyre 2001). The number of copulations vary during a mating bout in giant weta. Each one lasts about 1 h in the congeneric D. heteracantha and D. fallai, and during it a single spermatophore is produced and transferred to the female where it is inserted beneath her subgenital plate (Richards 1973). The male then releases the subgenital plate, and during the next few minutes the spermatophore is gradually forced out of the female by the pushing movements of the male’s paraprocts and attempted copulations (Richards 1973). The externally positioned spermatophores are not eaten (as in most ensiferan orthopterans; Brown and Gwynne 1997). Deinacrida rugosa exhibits striking sexual size dimorphism (see ‘‘Results’’ below). In addition to intersexual variation, there is also substantial size variation within the
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sexes. Some of this variation in size appears to be under strong selection in males, where light bodies and long legs appear to be favored in scramble competition for access to females (Kelly et al. 2008). Although selection on female size has not been formally measured in this species, there is a general expectation of fecundity selection for large mass in insects with female-biased size dimorphism (reviewed in Blanckenhorn 2005). In this field study, we examine whether and how these selection pressures result in size assortative mating in D. rugosa. In addition, because we can estimate ejaculate investment in the wild for this species (i.e. empty spermatophore casings are easily counted after a mating bout), we examine how the body size of each member of a mating pair relates to the average ejaculate size of the male. One hypothesis is that, given the time investment in a mating, males preferentially associate with large females in order to take advantage of their presumably increased fecundity. If small males win in scramble competition for these large females (Kelly et al. 2008), the prediction is a negative assortative mating pattern. Alternatively, males may exercise their choice during copulation by allocating more sperm (i.e. additional spermatophores) to larger and more fecund females. Although this response to the presumed greater intensity of sperm competition in matings with large females is common (Reinhold et al. 2002), another possible outcome is that males maximize their fertilization success by investing fewer sperm in matings with non-virgins as is known across insect species (C.D. Kelly and M.D. Jennions, metaanalysis in preparation).
Materials and methods Study species and field site Our study was conducted over 4 years: February 2001, March–May 2002, April 2004, and April–May 2006 on Te Hoiere/Maud Island, New Zealand (41°020 S, 173°530 E), a 309-ha scientific reserve free of alien predators [e.g., rodents (Mus and Rattus spp.) and stoats (Mustela erminea)] (see also Kelly 2005b, 2006). Marking and measuring study animals In each year, we opportunistically collected adult giant weta by scanning the open ground and pastures at night. For each individual captured, we noted its sex and developmental stage (juvenile or adult). By using digital callipers (Mitutoyo Digimatic, Toronto, Canada), we measured each adult to the nearest 0.01 mm for each of left and right hind tibia (all years except 2004) and hind femurs (2001) in
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addition to pronotum width (2004 and 2006 only). Body mass was measured to the nearest 0.25 g with a 30 g Pesola scale (2001–2003) or to the nearest 0.10 g using an electronic field balance (2004 and 2006). We also marked every censused animal with a uniquely numbered and coloured bee tag (H. Thorne, Market Rasen, UK). In 2006, we also glued (cyanoacrylate) 0.40-g radio transmitters (PIP3; Biotrack, Dorset, UK) to the pronota of a subset of individuals with the antenna pointed backwards (transmitters were removed 3–4 days later). Radio-tagging does not bias the movements of giant weta as the smallest tagged individuals (smaller males) move significantly greater distances each night than tagged weta with larger body sizes (females and larger males) (Kelly et al. 2008). After processing (which took ca. 5 min on average), each animal was released at its point of capture.
we released the animals at their point of capture. In 2006, radio-tagging allowed us to leave pairs to mate in their natural refuges at the base of vegetation for later relocating and recovery (see Kelly et al. 2008 for details of methods). Thus, if a radio-tagged individual was paired, we inspected the refuge and both individuals for spermatophores near dusk, the time at which pairs typically separate and decamp. A greater error in counting spermatophores might be expected in the field situation because of the loss of spermatophores in the conditions of the natural refuge; however, this did not appear to be a problem as the numbers of spermatophores transferred by males of a given body size did not differ between our methods of measuring insemination success (i.e. matings that occurred in the natural refuge vs matings in plastic buckets; see heterogeneity of slopes test, below).
Size assortative mating
Statistical analysis
We noted whether individuals captured in 2001 and 2004 were in close contact with a member of the opposite sex. For giant weta species, it is generally true that a male in close contact with a female throughout the night mates with her the subsequent day (we observed marked males following and remaining in contact with marked females for several hours) (Richards 1973; McIntyre 2001). We determined how each of the four phenotypic traits covaried between males and females.
All morphological variables were log10-transformed prior to analysis. We assessed whether data collected in different years could be pooled by performing heterogeneity of slopes tests with year included as an independent variable (fixed effect) in the model. As the interaction term (i.e. morphological variable of interest 9 year) was never significant at B0.05 (i.e. similar slopes), the data were then pooled across years for all relevant tests. Pearson productmoment correlation was used to calculate r. In our examination of correlates of pairing success and spermatophore transfer, we performed separate bivariate analyses for each sex because different traits were measured in different study years. Untransformed means are given ±1SE of the mean and correlation coefficients (effect sizes) are presented with 95% confidence intervals (see Nakagawa and Cuthill 2007 for methods).
Phenotypic correlates of pairing success and spermatophore transfer Once a male locates a receptive female, he remains in physical contact with her using either his antennae or legs, and follows her until she finds a diurnal refuge (Richards 1973; McIntyre 2001). Radio-tagging allowed us to locate individuals while they were in their diurnal refuges and thus obtain information on whether they were with a member of the opposite sex. By tracking the movements of individuals for several days, we were able to calculate pairing success as the proportion of observations in which an individual was in contact with a member of the opposite sex. Remating data were available for 2006 only. In all years of our study, pairs found at night (male and female less than one body length apart) in which neither pair member was radio-tagged were placed into plastic tubs (ca. 17 9 17 9 10 cm) lined with fresh grass. The tubs were then either brought into the laboratory (2001–2003) or left at the location of capture until the following night (2004 and 2006). After 24 h, we inspected both individuals as well as the plastic tub for used spermatophores. The number of spermatophores gave an estimate of the individual’s insemination success. After counting the spermatophores,
Results Sexual size dimorphism All phenotypic traits were significantly correlated within each sex (Table 1). Females were significantly larger than males for each of the four measured traits with body mass showing the greatest degree of difference: females were approximately twice as heavy as males (Table 2). Size assortative mating Of the four traits measured for members of mating pairs (Table 3), tibia length exhibited the strongest correlation between the sexes (r = 0.34), although this relationship was statistically non-significant (P = 0.063). For the other
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Table 1 Phenotypic correlations (r) of Deinacrida rugosa, between traits with each sex (all P values \0.05) Females
Males Body mass (g)
Tibia length (mm)
Body mass (g)
Femur length (mm)
0.59 (106)
Tibia length (mm)
0.53 (145)
Femur length (mm)
0.63 (104)
0.74 (104)
Pronotum width (mm)
0.56 (102)
0.86 (41)
Pronotum width (mm)
0.74 (55)
0.70 (101)
0.78 (55)
0.70 (51) –
–
Numbers in parentheses denote sample size, and dashes represent cases in which traits were not measured in the same study year Table 2 Sample size, mean and coefficient of variation (CV) for absolute values of body mass (g) and size (mm) in male and female Deinacrida rugosa on Maud Island, NZ Trait
Male
Female
Mean ± SE Body mass (g)
CV
n
Mean ± SE
CV
Dimorphism (% difference)
F
df
n
9.78 ± 0.16
20.33
156
18.35 ± 0.27
20.78
206
?46.70
832.6
1,360
Tibia length (mm)
28.94 ± 0.16
5.87
106
31.74 ± 0.19
7.08
145
?8.82
108.5
1,249
Femur length (mm)
26.74 ± 0.17
4.65
55
29.40 ± 0.16
5.55
104
?9.05
108.4
1,157
Pronotum width (mm)
14.94 ± 0.09
6.20
104
17.34 ± 0.11
6.67
103
?13.84
292.7
1,207
F values and df are from one-way ANOVA on log10-transformed data testing for a sex difference in each trait (all F values P \ 0.0001). Positive values for dimorphism denote female-biased dimorphism Table 3 Correlation (Pearson’s r) for each of four phenotypic traits of field-collected male–female pairs of D. rugosa
Table 4 Correlation (Pearson’s r) between each of four male traits and pairing success and the number of spermatophores transferred by males during a single mating bout
Trait
r (95% CI)
n
Tibia length (mm)
0.34* (-0.016 to 0.619)
31
Femur length (mm)
0.23 (-0.136 to 0.604)
31
-0.07 (-0.389 to 0.264)
36
Tibia length
67
Body mass -0.40* (-0.640 to -0.086) 37 Pronotum width -0.35** (-0.602 to -0.034) 38
Male trait
Pronotum width (mm) Body mass (g)
-0.03 (-0.268 to 0.211)
* P = 0.063
In 2006, mating pairs were kept during the day either in a plastic bucket or left in situ. Heterogeneity of slopes tests showed that the housing environment during mating did not affect the relationship between the number of spermatophores transferred by males and either trait measured (tibia length 9 environment: F1,28 = 0.09, P = 0.93; body mass 9 environment: F1,28 = 0.04, P = 0.84; pronotum width: F1,28 = 0.30, P = 0.59). Therefore, we pooled these data. Our hypotheses (see ‘‘Introduction’’) assume that body size in males does not limit spermatophore production. This appears to be the case as we detected no significant effect of any male trait on the number of spermatophores
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n
Partial r n
Pairing success (2006)a -0.10 (-0.406 to 0.227)
38
Spermatophore transfer (2001, 2002, 2004 and 2006)a
three aspects of phenotype, only femur width, another aspect of leg morphology, gave any hint of either positive or negative association. Male correlates of spermatophore transfer
r (95% CI)
Tibia length
-0.008 (-0.301 to 0.371)
49
0.14
17
Femur length
-0.17 (-0.601 to 0.338)
17
0.10
17
Body mass
-0.15 (-0.347 to 0.06)
89 -0.15
53
Pronotum width
-0.15 (-0.385 to 0.083)
73 -0.18
33
Partial r is the correlation once female phenotype has been accounted for. Sample sizes are smaller for partial r because it includes only those cases in which both mating partners were measured. Partial r was not calculated for pairing success because the identity of only one individual of a mated pair was known * P = 0.015 ** P = 0.031 a
The year(s) in which data were collected
that males transferred to females during a single mating bout either with (partial r) or without statistically controlling for female size (Table 4). Female correlates of mating and spermatophore transfer As for males, housing environment did not affect the relationship between the number of spermatophores
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Table 5 Correlation (Pearson’s r) between each of four female traits and pairing success and the number of spermatophores transferred by males during a single mating bout Female trait
r (95% CI)
n
Partial r
n
Pairing success (2006)a Tibia length
0.24 (-0.162 to 0.574)
25
Body mass Pronotum width
0.33 (-0.066 to 0.636) 0.32 (-0.077 to 0.629)
25 25
Spermatophore transfer (2001, 2002, 2004 and 2006)a Tibia length
-0.03 (-0.355 to 0.301)
36 -0.18
17
Femur length
-0.03 (-0.553 to 0.493)
17 -0.23
17
Body mass Pronotum width
-0.29* (-0.534 to -0.062) 72 -0.28** 53 -0.22 (-0.453 to 0.049)
56 -0.13
33
Partial r is the correlation once male phenotype has been accounted for. Sample sizes are smaller for partial r because it includes only those cases in which both mating partners were measured. Partial r was not calculated for pairing success because the identity of only one individual of a mated pair was known * P = 0.014 ** P = 0.044 a
The year(s) in which data were collected
received by females and either measured trait (tibia length 9 environment: F1,17 = 0.08, P = 0.93; body mass 9 environment: F1,17 = 0.04, P = 0.85; pronotum width: F1,17 = 0.59, P = 0.45). Therefore, data collected from females in tubs and in situ were pooled for each trait. Heavier females received fewer spermatophores during a single mating bout, both with (partial r) and without statistically controlling for male size (Table 5). Although the relationships between female phenotypic traits and of male partners were not statistically significant, the correlation coefficients for these relationships were of similar magnitude (body mass: r = 0.33 and pronotum width: r = 0.32) to the coefficients for the covariation between body mass and number of transferred spermatophores (r = -0.29).
Discussion Our results did not support the hypothesis that small male winners of scramble competition (Kelly et al. 2008) that should prefer larger, more fecund mates ejaculated more sperm with these females; there was no evidence of allocation of more spermatophores to large mates. This result counters many empirical studies that show increasing numbers of sperm are donated to larger (higher quality) females (e.g., Yusa 1994; Gage and Barnard 1996; Mallard and Barnard 2003). There was also no evidence of negative assortative mating. Our findings
were more consistent with the alternative scenario that small male winners of sexual competition invest more sperm with small females. Males pass significantly more spermatophores during a single mating bout to lighter females as well as those having a smaller body size; female mass and pronotum width explained approximately 8 and 5% of the variation in the number of spermatophores they received, respectively. That males pass more spermatophores to lighter females could be either the hypothesized adaptive response by males to the sperm competition risk posed by larger females or could be a result of male sperm depletion. We discuss each hypothesis in turn. First, if larger females pose a greater risk (or intensity) of sperm competition because they experience greater mating success (perhaps due to having higher fecundity), then by transferring more spermatophores to smaller females (less risk), males may maximize their fitness (Parker et al. 1996, 1997; Wedell et al. 2002; Engqvist and Reinhold 2005). Our observation that larger females (i.e. heavier and wider pronotum width) have greater pairing success than lighter females supports this hypothesis. This result, however, must be interpreted cautiously as the finding was not statistically significant but rather, the effect sizes (body mass: r = 0.33 and pronotum width: r = 0.32) were large and of similar magnitude to the significant relationship between female size and the number of spermatophores received (r = -0.29). We suggest that, since females climb atop males during copulation, males may be able to assess female weight, and in turn, assess their risk of sperm competition. Alternatively, perhaps males do not adaptively allocate sperm, and the observed pattern of spermatophore transfer is simply a case of those males that mate heavier females being sperm depleted. This should arise if the males that mate most frequently (and thus become depleted) also tend to mate heavier females. This does not appear to be the case in D. rugosa as lighter males have higher pairing success (and insemination success; Kelly et al. 2008). Furthermore, because there is an apparent lack of negative assortative mating based on body mass, lighter males do not mate heavier females more often. The explanation for negative covariance between female size and spermatophore transfer thus remains elusive. We found weak support for positive size assortative mating in Deinacrida rugosa as there was a marginally non-significant association between the tibia lengths of pairs. Tibia length explained approximately 12% of the variation in the observed mating pattern; an effect size nearly double that typically found in evolutionary ecology studies (Møller and Jennions 2002). Although the correlative nature of our study does not allow us to identify the causal mechanism responsible for the observed pairing
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pattern, our previous work on this species (Kelly et al. 2008) suggests an explanation based on individual mobility. Kelly et al. (2008) found that males having longer legs, smaller pronotum width and smaller body mass travelled greater distances per night. Therefore, the positive assortative mating by tibia length suggested by our data could be due to males with longer tibia being superior competitors in scrambles for larger, more fecund females (tibia length and body size are positively correlated in females). An alternative, but not mutually exclusive, hypothesis is that tibia lengths are phenotypically correlated with some other unmeasured trait that is the basis for the association between similar individuals. In addition to identifying how particular phenotypic traits in males and females relate to pairing and insemination success, our results highlight the extreme sexual size dimorphism in Deinacrida rugosa. We found that adult males of this species of giant weta are only about half the mass of adult females. The magnitude of size dimorphism in D. rugosa (47%) is greater than that exhibited by several other Deinacrida species (C.D. Kelly, unpublished data; McIntyre 2001) as well as most birds (Sze´kely et al. 2000), mammals (Lindenfors et al. 2002; Thoren et al. 2006), spiders (Prenter et al. 1999), and insects (Teder and Tammaru 2005). However, the degree of dimorphism in body size exhibited by D. rugosa is similar to the degree of dimorphism in weapon size (mandible length used in fights between males) found in another deinacridine weta, the Wellington tree weta, Hemideina crassidens (Kelly 2005a). A better understanding of how sexual selection operates in this size-dimorphic giant insect is beginning to emerge; however, many questions remain unresolved. Primary among these is a better understanding of the evolution of size dimorphism, including addressing the role of body size in pair formation and factors determining the number of spermatophores transferred to females. Answering these questions will require not only better knowledge of giant weta behavior and demographics but also determining the risk of sperm competition typically experienced by males and quantifying the relationship between female body size and fecundity. Acknowledgments We thank Karen Mayhew and Steve Ward (New Zealand Department of Conservation, Marlborough Sound) for assistance while this research was being conducted on Maud Island. While on the island, Leigh Joyce also kindly helped us with radio˚ sa Berggren telemetry. We greatly appreciate the time and effort A and Matt Low volunteered to this study. Ian Millar (New Zealand Department of Conservation, Nelson) kindly arranged research permits. This research was supported by grants from the National Science and Engineering Research Council (NSERC) of Canada and National Geographic Society to D.T.G., NSERC Postdoctoral Fellowships to each of L.F.B. and C.D.K., a UNSW Faculty Research Grant to L.F.B. and Robert Brooks, a travel grant from the Swiss Academy of Natural Sciences to L.F.B.
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