Colony size is linked to paternity frequency and paternity skew in yellowjacket wasps and hornets
© Loope et al.; licensee BioMed Central. 2014
Received: 29 June 2014
Accepted: 18 December 2014
Published: 30 December 2014
The puzzle of the selective benefits of multiple mating and multiple paternity in social insects has been a major focus of research in evolutionary biology. We examine paternity in a clade of social insects, the vespine wasps (the yellowjackets and hornets), which contains species with high multiple paternity as well as species with single paternity. This group is particularly useful for comparative analyses given the wide interspecific variation in paternity traits despite similar sociobiology and ecology of the species in the genera Vespula, Dolichovespula and Vespa. We describe the paternity of 5 species of yellowjackets (Vespula spp.) and we perform a phylogenetically controlled comparative analysis of relatedness, paternity frequency, paternity skew, colony size, and nest site across 22 vespine taxa.
We found moderate multiple paternity in four small-colony Vespula rufa-group species (effective paternity 1.5 – 2.1), and higher multiple paternity in the large-colony Vespula flavopilosa (effective paternity ~3.1). Our comparative analysis shows that colony size, but not nest site, predicts average intracolony relatedness. Underlying this pattern, we found that greater colony size is associated with both higher paternity frequency and reduced paternity skew.
Our results support hypotheses focusing on the enhancement of genetic diversity in species with large colonies, and run counter to the hypothesis that multiple paternity is adaptively maintained due to sperm limitation associated with large colonies. We confirm the patterns observed in taxonomically widespread analyses by comparing closely related species of wasps with similar ecology, behavior and social organization. The vespine wasps may be a useful group for experimental investigation of the benefits of multiple paternity in the future.
The mating frequency of social insect queens is a central factor shaping the evolution of social behavior within colonies. Polyandry, and the genetic diversity created by multiple paternity, is the foundation of many evolutionary conflicts within insect societies . It also has important consequences for sexual selection, sperm competition, and the evolution of male reproductive strategies ,. But the evolution of multiple mating and multiple paternity itself is an evolutionary puzzle. It has arisen several times in the social Hymenoptera, including in a handful of ant genera, the honey bees (Apis spp.), and some vespine wasps (e.g. Vespula spp.) . Multiple paternity presents automatic costs of increased exposure to sexually transmitted disease, greater predation risk while mating, and greater potential conflict among colony members due to lower relatedness . So, given these costs, what are the benefits that underlie the adaptive maintenance of multiple paternity?
Comparative analyses have shown that across taxonomically broad sets of species, there is a positive relationship between paternity frequency and colony size ,,, as well as a negative relationship between paternity skew and paternity frequency, in ants, bees, and wasps . As the selective forces that drive the evolution of polyandry may differ across the social insects , our aim in this work is to examine these predictions in a clade possessing a wide range of paternities, with species that differ little in social complexity and other traits that might confound the explanation of multiple paternity.
For the vespine wasps, we extend the logic of the pathogens hypothesis to propose another factor–nest site–that may be involved in the evolution of multiple mating and multiple paternity. Vespine wasps all construct similar nests of multiple combs surrounded by insulating layers of paper envelope (Figure 1). Some species build nests hidden in cavities, typically excavated rodent burrows, rotten logs or tree holes. Other species construct exposed, aerial nests in shrubs or suspended from tree branches. It seems possible that these nest sites, and their microenvironments, expose colonies to different types and quantities of pathogens, as has been suggested for canopy- and soil-dwelling ants . Cavity-nesting and ground-nesting species may experience greater exposure to fungal and other microbial pathogens due to the increased proximity to damp soil and rotting wood, which could in turn favor multiple paternity. A casual examination of the vespine species included in the most extensive comparative analysis of colony size and paternity  suggests an association between colony size, nest site, and paternity. The large-colony, vulgaris-group Vespula species are subterranean nesting and have high paternity, while the small-colony Dolichovespula species are aerial nesting and have a low paternity. Because nest site and colony size are tightly associated in this data set, it is unclear whether it is colony size or nest site (or both) that distinguishes high-paternity species from low-paternity species.
Here we assume that colony size and nest site are determined by ecological factors , such as climate, prey type and availability, nest site availability and predator type and abundance. These hypotheses predict that selection then modifies mating and paternity traits to reflect the ecologically determined colony size and nest site. In short, these hypotheses predict that colony size and nest site cause changes in mating behavior and paternity, rather than vice versa (Figure 2).
In this study we describe the paternity of five species of North American Vespula wasps. Four of these species are members of the enigmatic Vespula rufa group, which have small colonies and subterranean nests ,. These features make this clade attractive for testing the link between nest site and paternity as these species break the correlation between colony size and nest site found in the species that have been previously studied. The fifth species, Vespula flavopilosa, has small colonies compared to other species in the Vespula vulgaris group , and may thus provide an interesting intermediate position in the comparison of colony size and mating frequency. It is also a facultative social parasite , a feature sometimes associated with reduced paternity ,. We then perform a phylogenetically controlled comparative analysis, including both colony size and nest site, to examine the species-level traits associated with the evolution of intracolony genetic similarity (relatedness), paternity frequency and paternity skew in the Vespinae.
We collected workers from active, mature colonies located by responding to pest control calls (V. consobrina, V. atropilosa and V. acadica in Thurston, Co., WA), by nest searching (V. flavopilosa; Tompkins Co., NY), or by “wasp-lining” foragers back to their nests (V. vidua; Tompkins Co., NY). All collections adhered to state and federal regulations. Most colonies would have been destroyed as pests regardless of our collection, and none are species known to be endangered or threatened. Samples were collected between 2008–2013 and stored frozen (−20 deg C). We collected entire colonies of V. consobrina, V. vidua and V. flavopilosa to obtain colony size data; a sample of worker V. acadica and V. atropilosa were collected from the nest entrance with a vacuum. All V. consobrina and some V. vidua colonies were collected during the day using a battery-powered vacuum. The collector waited at least 30 minutes to collect returning foragers, and for V. vidua, we returned hours later to collect the last remaining foragers and escapees. All colonies of V. flavopilosa and some colonies of V. vidua were anesthetized overnight with CO2 and excavated in the morning. For colonies of V. consobrina, V. vidua and V. flavopilosa, we counted all adult workers and determined the presence or absence of the mother queen.
We extracted DNA from approximately twenty workers or gynes per colony, as well as the mother queen when present, by placing a single antenna or leg in 100 μL of 10% Chelex solution (Chelex 100, 100–200 mesh, Bio-Rad), then incubating for 20 minutes at 95°C. We then refrigerated or froze the supernatant before PCR. Variable loci were selected based on preliminary screening of published loci -. We used dye-labeled primers (Applied Biosystems) in combination with a 3-primer labeling method  to perform multiplex PCR with 4–6 primers, depending on the species (Additional file 1: Table S1). Each 10 μL PCR reaction included 1ul extracted DNA, 5 μL Qiagen master mix (Qiagen Type-It Microsatellite Kit, Qiagen Inc.), 0.2 μL of each reverse primer, 0.2 μL (dye-labeled) or 0.1 μL (3-primer labeled) of each forward primer, 0.15 μL FAM-labeled 3-primer tag for each 3-primer-labeled primer pair, and water to total 10 μL. PCR reaction conditions were 95°C for 15 minutes, 35 cycles of 95°C for 30 seconds, 50°C for 90 seconds, 72°C for 60 seconds, followed by 60°C for 30 minutes. Fragment analysis was performed on an ABI-3730 × l sequencer using 0.5 μL PCR product combined with 15 μL HiDi Formamide and 0.15 μL LIZ 500 internal size standard (Applied Biosystems). Allele sizes were called using GeneMarker (SoftGenetics LLC) and checked twice by eye.
We used Colony2 v220.127.116.11  to find the maximum likelihood configuration of paternity assignments for all genotyped workers. Workers that failed to amplify at more than two loci were excluded from the analysis. In the few cases where Colony2 assigned a worker to a matriline from a different colony, the anomalous worker genotype was checked against the genotype of the queen from that colony. If she shared an allele with the queen at all loci, a maternal sibship constraint was entered into Colony2 containing all workers in that colony that did not differ from the queen for both alleles at any locus. In all cases, the subsequent run of the likelihood analysis assigned the worker to an additional patriline from that colony. In the few cases where anomalous workers were inconsistent with being a daughter of the queen, these workers were removed from the dataset and the analysis was run again. From the paternity assignments, we calculated each colony’s observed paternity frequency (k), an uncorrected estimate of effective paternity: where p is the proportion of offspring in the sample fathered by male i ,,, and a corrected estimate of effective paternity (k e3 ), which adjusts for sample size . Mean intracolony relatedness was calculated from effective paternity using the formula . We calculated paternity skew using the B index . Additional file 1: Table S1 reports allelic diversity and expected heterozygosity calculated from allele frequencies determined by Colony2.
Non-detection and non-sampling error
Summary data from paternity analysis of five Vespula species
19.9 (19, 20)
2.00 (1.42, 2.58)
1.47 (1.17, 1.98)
1.51 (1.18, 2.08)
4.7e-4 a (1.3e-3) b
20.1 (19, 23)
2.40 (1.80, 3.00)
1.67 (1.37, 2.14)
1.72 (1.39, 2.26)
2.5e-3 a (1.3e-2) b
20.4 (18, 24)
2.83 (2.00, 3.66)
1.82 (1.43, 2.50)
1.89 (1.46, 2.68)
19.8 (18, 21)
3.00 (2.12, 3.88)
2.01 (1.62, 2.67)
2.12 (1.67, 2.90)
1.7e-5 a (4.1e-5) b
19.6 (18, 20)
3.80 (3.10, 4.50)
2.80 (2.34, 3.49)
3.07 (2.50, 3.97)
Non-sampling error occurs when a father is not detected because the sampled daughters do not include his offspring. We used the formula presented in , to estimate the expected number of patrilines per colony, given the observed number of patrilines and the number of individuals sampled, assuming no skew among patrilines. The species-level average expected paternity frequencies were virtually identical to the observed values (V. acadica: 2.00, V. atropilosa: 2.40, V. vidua: 3.02, V. consobrina: 2.85, V. flavopilosa: 3.84; compare to observed values in Table 1). Our estimates of effective paternity and thus relatedness are already corrected for non-sampling, since the calculation of ke3 accounts for non-sampling error . The values of ke3 were typically only slightly larger than k e (Additional file 1: Table S2), further suggesting that our sample sizes were sufficient to describe paternity in these species.
To analyze how mean colony size parameters and nest site preference influence paternity frequency, paternity skew, and resulting intracolony genetic similarity (relatedness), we compared these traits across 22 vespine taxa, including 2 subspecies. Because species are not independent due to shared ancestry, we performed our analyses using methods accounting for phylogeny ,.
We searched the literature for all vespine species with reports of paternity based on genetic data. We recorded the arithmetic mean number of patrilines per colony and used harmonic mean effective paternity to calculate intracolony genetic similarity (r). Where possible, we acquired colony-level paternity distribution data from authors to calculate the species mean B index of paternity skew for colonies with multiple paternity . We then searched for data on average and maximum mature colony size (worker number). For species with multiple reports of colony size or effective mating frequency, we chose the study with the largest sample size, attempting to use reports of the two variables from the same population whenever possible, and (with the exception of Vespa velutina) only reports from colonies studied within the species’ native ranges. Our goal was to describe the average peak colony size of each species. Because colony sizes vary over the season, whenever possible we used averages of colonies that had adult reproductives present but had not entered decline (see Additional file 2). We similarly found data on the maximum number of workers recorded in an annual colony of each species, for colonies within the species’ native range. Finally, we also found estimates of the nest-site preferences of each species, recording the fraction of colonies with enclosed or subterranean nests (as opposed to aerial, exposed nests).
We generated a phylogenetic hypothesis for our dataset using phyloGenerator  based largely on molecular data reported in two recent studies of vespine phylogeny , (Genbank accession numbers available in Additional file 1: Table S5). Sequences were aligned with MAFFT v6.847b , and the phylogeny was estimated with RAxML 7.3.0  using a GTRGAMMA model and a single ML run with 1000 integrated bootstraps to determine support. We ultrametricized the resulting tree using the chronopl function in the R package ape with λ = 0 to approximate non-parametric rate smoothing . Three species with trait data (Vespula rufa, V. atropilosa, and D. norwegica) were omitted from the analysis because no sequence data were available. Although our resulting tree closely matched the topology for Vespula and Dolichovespula of Lopez-Osorio et al. , the additional data used by Perrard et al.  led to a topology for Vespa that differed from ours. To ensure that this difference did not influence the outcome, we performed the same comparative analysis on a tree with a Vespa topology consistent with Perrard et al.  and all branch lengths set equal to 1.0  (Additional file 1: Table S3, Additional file 1: Figure S1).
Because species data are not independent due to shared history , we analyzed comparative data with phylogenetic generalized least squares (PGLS) models  implemented in R version 3.0.3 using the caper package ,. To improve homoscedasticity we log-transformed colony size and inverse-transformed the skew index B. In each model we determined how well colony size and nest site predict intracolony genetic similarity (r), paternity frequency (k) or paternity skew (B), while accounting for phylogenetic history. We also performed a similar analysis using the maximum observed colony size rather than mean colony size for each species (Additional file 1: Table S4). In PGLS models, branch lengths of a phylogeny are used to correct for the non-independence of regression residuals, the basic assumption of ordinary least squares models that is violated by species data. The transformation parameter λ scales the branch lengths of the phylogeny and thus the degree to which the phylogeny affects the regression’s residuals. When λ = 0, the phylogeny is scaled to a star phylogeny and the analysis is equivalent to an ordinary least squares model. When λ = 1, PGLS is equivalent to Felsenstein’s independent contrasts , the most conservative analysis allowing the greatest effect of phylogeny. Using maximum likelihood methods, λ can be optimized to best fit the residuals of the regression model . We ran each model twice, once with the maximum likelihood value of λ and, because the likelihood surfaces were often shallow, once with λ set to the upper 95% confidence interval value for the maximum likelihood estimate, for the most conservative analysis (i.e., allowing the greatest effect of phylogeny). To confirm that residuals were distributed normally, residual density plots were checked by eye.
Results and discussion
The first aim of this study was to describe paternity in five species of Vespula wasps. The second aim was to determine if colony size and nest site predict intracolony genetic similarity (relatedness) across species, and if this pattern arises through effects of colony size and nest site on paternity frequency, paternity skew, or both. These patterns are used to address the question of why multiple mating and multiple paternity evolve.
All four species of the Vespula rufa group exhibited moderate multiple paternity, with most queens mating more than once, and some using the sperm from as many as 6 males (Additional file 1: Table S2). The estimated mean effective paternity values for species in the Vespula rufa group were moderate, varying between 1.5 and 2.1 (Table 1), and similar to V. rufa, which has a mean effective paternity of 1.5 . Consequently, these species may provide interesting fodder for investigating the evolution of worker reproduction: when effective paternity is near 2.0, relatedness is not predicted to determine whether workers favor worker- or queen-derived males, as their relatedness to these two types of males is equal . Thus, other factors such as costs of worker reproduction or the effectiveness of queen policing may usefully explain differences between these species. Behavioral observations suggest that such differences exist: some species appear to have frequent worker reproduction (e.g., V. rufa  and V. consobrina ), while others may have little or no worker reproduction in queenright colonies (V. acadica , V. atropilosa , and V. vidua, Chien and Loope, unpublished data).
The high average effective paternity of Vespula flavopilosa (~3.1) is similar to other members of the Vespula vulgaris group, though lower than other large-colony species in eastern North America . This suggests no reversion to low paternity due to facultative social parasitism, as was also found in the similar social parasite Vespula squamosa . This makes sense given that queens of both of these species eventually produce colonies with many workers, and thus likely benefit from greater paternity for the same reasons as other large-colony Vespula. It remains to be seen whether the rufa-group social parasite species (e.g., V. infernalis and V. austriaca), which lack a worker caste but are probably derived from a moderately polyandrous ancestor, have reverted to monandry as predicted by the hypothesis of benefits of a genetically diverse workforce ,.
The effects of colony size and nest site on paternity frequency and paternity skew
PGLS models of the effect of colony size and nest site on paternity traits across 22 Vespine taxa
λ = ML
log 10 ( size ) +
Paternity frequency (k)
log 10 ( size ) +
Paternity skew (B −1)
log 10 ( size ) +
λ = upper 95% CI
log 10 ( size ) +
Paternity frequency (k)
log 10 ( size ) +
Paternity skew (B −1)
Our PGLS models simultaneously estimate regression coefficients and optimize the error structure of the residuals using the λ transformation ,,, the recommended procedure for analyzing comparative data that may have phylogenetic signal. When λ is zero, the phylogenetic signal is estimated to be zero and the analysis is equivalent to ordinary least-squares regression, whereas when λ is set to 1, the model incorporates the maximum amount of phylogenetic covariance and is equivalent to independent contrasts analysis . The maximum likelihood estimates of λ from our models are low to moderate, between zero and 0.35, for models including both colony size and nest site (Table 2), though the uncertainty in the λ estimates suggests a possibly large phylogenetic signal. Regardless, the most conservative analyses (models with λ set to the upper 95% confidence interval) yield similar significant effects of colony size on relatedness, paternity frequency, and paternity skew (Table 2). The alternative analyses using a different phylogeny (Additional file 1: Table S3) or maximum size as a proxy for colony size (Additional file 1: Table S4) give similar results. Unsurprisingly, actual variation in paternity skew and paternity frequency both significantly predict intracolony relatedness (Table 2). Overall, these results are consistent with the hypothesis that colony size influences intracolony relatedness through changes in paternity frequency and paternity skew. These findings for the Vespinae are in concord with previous analyses of more phylogenetically diverse sets of species ,.
The evolution of multiple paternity in the Vespinae
We have considered the factors associated with the evolution of multiple paternity in a group of social wasps sharing similar annual life histories, colony founding strategies, natural enemies, temperate and subtropical distributions, foraging behaviors, and food sources ,,,. Our results confirm an important role of large colony size in the evolution of high paternity in this group. This pattern is based partly on the correlated independent origins of large colony size and high paternity in the vulgaris and squamosa groups (or a single such origin and then correlated reduction of colony size and paternity in the rufa group; Figure 3). It is also supported by transitions to moderate colony size and moderate multiple mating in the hornets, by Vespa simillima, Vespa velutina and Vespa affinis, though these groups are in need of more study. Further evidence for a link between colony size and paternity would come from confirming the difference reported between subspecies of V. simillima , and a detailed description of paternity and colony size for V. velutina in its native range.
What does the strong association with colony size tell us about the selective factors leading to multiple mating and multiple paternity in these species? The pathogens hypothesis is consistent with the observed effect of colony size, but remains to be directly tested in vespine wasps. The predictions that pathogens enter colonies via foragers, that larger colonies within species have more pathogens, and that species with larger colonies have more pathogens, are all testable. Numerous parasites and pathogens of social wasps have been identified ,, but studies of their relative occurrence and association with colony traits are lacking. The strongest evidence for this hypothesis come from experimental manipulation of mating frequency in bees ,. Such an experiment would provide a powerful test of this hypothesis in vespine wasps.
The colony size prediction of the division of labor hypothesis rests on the existence of a difference between small- and large-colony species in behavioral organization. This could be the case if large-colony species possess more morphological or behavioral castes, improved division of labor based on genetically determined task thresholds, or a larger behavioral repertoire . Such a pattern has been well documented in the polistine wasps, with greater specialization and evidence supporting a genetic basis underlying specialization, in large-colony species -, as well as differences in task partitioning within species according to colony size . However, there is little evidence for such a difference in the Vespinae . Large-colony Vespula workers typically lack long-term specialization ,, and there is no evidence that they possess more complex, coordinated behaviors such as recruitment signals or task partitioning of nest construction . On the other hand, studies of the division of labor and specialization in these wasps are few, and overlooked specialization or complexity in large-colony species, consistent with the division of labor hypothesis, may yet be discovered.
A third popular hypothesis, that queens require multiple mates to obtain enough sperm to last a lifetime ,, also predicts an association between multiple paternity and colony size. However, this hypothesis does not predict that queens of large-colony, highly polyandrous species use males’ sperm more evenly than their small-colony, slightly polyandrous counterparts (Table 2; ). Queens that are sperm limited should use all available sperm, and thus paternity skew should reflect the (presumably high) variation in male sperm availability. Therefore, our data suggest that selection for increasing genetic diversity, rather than selection to increase sperm quantity, may explain high paternity in the vespine wasps.
Additional hypothesized benefits of high paternity, such as reducing sex ratio conflict , or obtaining rare, critical patrilines ,,, are not obviously linked to colony size, and thus seem less likely to explain multiple paternity in the vespine wasps. However, this group may provide useful subjects for further tests of these and other hypotheses, once more is known about their natural enemies, division of labor, mating biology, and sex investment. It will also be valuable to explore an alternative explanation for a link between colony size and paternity not considered here: it may be that increased paternity reduces intra-colony conflicts, increasing productivity and resulting in larger colonies ,,.
Our results show a strong association between colony size, paternity frequency and paternity skew in the vespine wasps, consistent with earlier, taxonomically broad, analyses. The observed patterns are consistent with hypotheses for the benefits of multiple paternity based on intracolony genetic diversity, but do not support the sperm limitation hypothesis. Clearly, further, more direct, tests of the pathogens hypothesis and the division of labor hypothesis are needed. Comparing closely related species with dramatically different paternity traits but otherwise similar natural history will help to reveal the details of when and why multiple paternity evolves.
Availability of supporting data
In Additional file 2 we provide details of metadata and sources used for the comparative analysis. In Additional file 3 we provide the genotypes used in paternity assignments. In Additional file 4 we provide the sequences, alignments and tree from our phylogeny. Genbank accession numbers are found in (Additional file 1: Table S5).
We are grateful to T. Seeley, K. Reeve and P. Sherman for support and advice throughout the study. We thank J. Kapoor and S. Bogdanowicz for advice on microsatellite genotyping. M. Choudhury helped with DNA extraction; and N. Mason and E. Hunter gave advice on comparative statistical analyses. We thank T. Seeley, H. Mattila, R. Jeanne, and M. Smith, as well as R. Jaffe and K. Foster, for comments that greatly improved the manuscript. We are grateful to K. Foster, M. Goodisman, and T. Wenseleers for providing us with data necessary to calculate paternity skew, and to R. Jaffe for suggesting the skew analysis. Funding for microsatellite primers came from a NSF-DDIG to KJL, and further funding for lab work came from an Animal Behavior Research Grant from the Cornell University Department of Neurobiology and Behavior to KJL.
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