Abstract
The Eurasiatic Polistes nimpha belongs to primitively eusocial wasps for which no data are available on its population’s genetic structure and relatedness/relationships of individuals. The purpose of this research is to determine the amplification efficiency in P. nimpha of microsatellite primers developed for P. dominula and using these primers, to explore genetic diversity, population structure and relatedness/relationship of P. nimpha in the context of its reproductive options. Eight out of twelve microsatellite markers analyzed on 59 individuals (pupae and larvae) were polymorphic (mean PIC = 0.545) and mutated following the stepwise mutation model. The Bayesian clustering method gave the probability of >0.898 of there being 10 clusters within the pooled sample of 15 nests. In two or three nest clusters, full- and/or half-siblings and unrelated individuals occurred. A significant correlation between genetic and geographic distances was detected. There are three main possibilities that come into play to explain our genetic results and direct field observations: cooperative nest foundation, visitations, and/or usurpation events. So far there is no conclusive evidence to exclude or support any of these possibilities.
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Introduction
The genus Polistes (Hymenoptera: Vespidae) comprises more than 200 wasp species representing a primitively eusocial group of insects (Carpenter 1996). Several factors have led to the intensive study of these species using either traditional (morphologic, behavioral and/or ecologic data) or molecular approaches. These are, for example, interesting population structure and genetics, a wide range of diversity in nesting habits and life cycle, and their role in ecosystems (Pardi 1948; Ono 1989; Sayama and Takahashi 2005; Hughes et al. 2008; Miyano et al. 2010; Nagamati Jr. et al. 2010; Tsuchida et al. 2014).
There are a limited number of studies that have been devoted to identification and the analysis of microsatellite loci in Polistes (Strassmann et al. 1997; Henshaw 2000; Saigo and Tsuchida 2010; Henshaw et al. 2011; Uddin and Tsuchida 2011; Komatsu et al. 2012). Here, for the first time, we performed microsatellite analyses of genetic diversity and structure of the population of Eurasiatic Polistes nimpha (Christ 1791) (Polistinae).
Polistes nimpha is one of the three species of the genus that can be found in Poland (Oleksa and Wiśniowski 2005). Small nests of this species are located on dead stalks of plants predominantly from the Apiaceae and Hypericaceae families, less often on small trees or on blades of grass (up to 50 cm aboveground surface).
The life cycle of P. nimpha is similar to that of the other representatives of the genus Polistes (see West-Eberhard 1969; Wilson 1979). Spring foundresses of Polistes wasps can make different choices regarding reproductive options (e.g., Seppä et al. 2012). Besides haplometrotic nest foundation (nest is founded by a single foundress), pleometrotic nest foundation (nest is started by several queens) is a widespread phenomenon among many species of Polistes (Makino and Sayama 1991). The results obtained so far indicate, that in the majority of cases Polistes colonies are founded by a single foundress (Miyano and Hasegawa 1998; Sayama and Takahashi 2005), but in P. nimpha pleometrotic nest foundation in sheltered places such as buildings was also noted (Cervo and Turillazzi 1985). Moreover, nest usurpation (queen replacement), either intra- or interspecific, in this species was observed (Cervo et al. 2004; Cervo 2006; Lorenzi et al. 2007). Although the other behavioral choices of foundresses during the pre-emergency period were described in P. dominula Christ 1791 (Nonacs and Revee 1995) and P. carolina (L. 1767) (Seppä et al. 2012), there is no evidence of visiting, deserting, switching, moving, adopting, or nest joining in P. nimpha. There is also no evidence of how reproduction is partitioned in the nest between queens and subordinate foundresses and/or potential joiners, movers, or adopters. Whether queens of P. nimpha mate with a single or multiple males also has not been tested (but see Turillazzi and Cervo 1982).
This study represents the first attempt to understand genetic diversity and population structure and relatedness/relationship between individuals of Polistes nimpha. The purpose of this research is twofold: (1) to determine the amplification efficiency and polymorphism of P. dominula microsatellites (Henshaw 2000) in P. nimpha and (2) to explore genetic evidence for possible reproductive options in this species.
Materials and methods
Study area
The study area was located at the edges of a military training field near the city of Poznań, Poland (Fig. 1). Three area plots (17,400; 5300; and 14,200 m2) where nest sites occur were selected in April 2014.
Nest searching and monitoring
Established plots were searched thoroughly for nests of P. nimpha. The initial nest searching began on May 12, 2014, and each recorded nest was revisited at approximately 7–10 (21)-day intervals. Nests were watched at forenoon hours 8:00 a.m. to 12:00 noon during the active hours of the inhabitants. One week after the nest identification, from May 19 to May 23, 2014, foundresses of P. nimpha were marked individually. Each nest was observed for 45 min per week during the following 5 weeks until days after the first workers’ appearances. Nest contents, a number of cells, and causes of nest failure were documented. Nests were considered as inactive if foundress was not present on the nest for two consecutive following checks. All nests have been marked with numbered tags. Moreover, the nest locations were measured at their latitude and longitude coordinates.
Sample collection
For genetic analysis, fifty-nine individuals were collected on June 9, 2014 from 15 nests (two pupae and two larvae per nest), except one nest from which one pupa and two larvae were taken. The pupae and larvae were preserved in 95 % alcohol and stored at low temperature (4 °C). Vouchers are deposited in the Department of Systematic Zoology, Faculty of Biology, Adam Mickiewicz University in Poznań, Poland.
DNA extraction and microsatellite amplification
Genomic DNA was extracted from the legs of each pupa (right leg of the second pair) or from ca. \( 1/3{-}1/2 \) of the larvae body using DNeasy Blood and Tissue Kit (Qiagen GmbH, Hilden, Germany) according to manufacturer’s instructions.
The PCR primers used were those developed for P. dominula (Henshaw 2000). PCRs were carried out in 5 μl reaction volumes containing 1× Type-it Microsatellite Kit (Qiagen), 0.07 μM forward primer, 0.2 μM reverse primer, 0.14 μM fluorescent-labeled M13 primer, and 1 μl (6–65 ng) of DNA template using a thermocycling profile of one cycle of 5 min at 96 °C followed by 30 steps of 30 s at 95 °C, 90 s at 50 °C, and 30 s at 72 °C, with a final step of 30 min at 65 °C.
Amplicons were fluorescently labeled in multiplexed reactions using a modified M13-tailing method (Oetting et al. 1995). The amplified alleles were separated on an ABI PRISM 3130XL (Applied Biosystems) with Genescan 600LIZ size standard and scored with the program Peak Scanner v 1.0 (Applied Biosystems).
Genetic diversity analysis
Genetic analyses were completed on a pooled sample of 59 individuals (pupae and larvae) collected from 15 nests. To describe informativeness of genetic markers related to expected heterozygosity, the polymorphism information content (PIC) values were calculated using the program Cervus. The program Micro-Checker v. 2.2.3 (Van Oosterhout et al. 2006) was used to test for the presence of null alleles, stuttering during the PCR amplification, and large allele dropout.
Genotype frequencies at any locus are a function of allele frequencies in the absence of migration, mutation, assortative mating, and natural selection. This situation is termed Hardy–Weinberg equilibrium. Deviations from this equilibrium can imply inbreeding, physical mixing of populations (Wahlund effect), population stratification, and/or null alleles. The deviation from Hardy–Weinberg proportions caused by heterozygote excess was tested with a global test (U test), as implemented in the program GenPop v. 4.2 (Raymond and Rousset 1995; Rousset 2008, http://kimura.univ-montp2.fr/~rousset/Genepop.htm), using 1000 dememorization steps, 100 batches, and 1000 iterations per batch. To assess the Hardy–Weinberg equilibrium for each locus, the goodness-of-fit Chi-square tests (Weir 1996) with Bonferroni correction, as implemented in the program Cervus v. 3.0.6., were performed.
To assign individuals to groups based on their multilocus genotypes, a Bayesian clustering algorithm was used, as implemented in the BAPS software version 6.0 at http://www.helsinki.fi/bsg/software/BAPS (Corander et al. 2008). The data were analyzed using a genetic admixture model for unlinked markers with the a priori upper bound for the number of clusters equal to 15. A principal coordinate analysis (PCoA), available in the program GeneAlEx v. 6.501 (Peakall and Smouse 2006, 2012, http://www.anu.edu.auG/BoZo/enAlEx) was conducted using Nei’s unbiased distance pairwise matrix to test whether patterns in microsatellite data support the partitioning of the sample into BAPS clusters.
As suggested by Frantz et al. (2009), it is important to test the analyzed data for isolation-by-distance before applying the Bayesian method of clustering. The relationship of genetic similarity and geographic distance is expected to be linear under the isolation-by-distance hypothesis (Rousset 1997). To check this hypothesis, a paired Mantel test (Mantel 1967) was performed for analyzed individuals with the program GeneAlEx. The test was based on linear genetic distances and geographic distances calculated on UTM coordinates of Lat./Log.; regression significance was tested with 999 permutations.
Kinship analysis, which relies on a model that assigns dyads to discrete relationship categories (Weir et al. 2006), was performed, based on three estimators: Wang’s (2002), Queller and Goodnight’s (1989) and the maximum-likelihood estimator (Kalinowski and Taper 2006). These estimators are implemented in the programs Coancestry v. 1.0.1.5 (Wang 2011) and ML-Relate (Kalinowski and Taper 2006). A correlation coefficient (r) was calculated to measure associations between the relatedness estimators using Statistica v. 10.0 (Statsoft). A t test was performed with the same program to determine whether differences between means of relatedness are significant between distinguished groups.
Results
Systematic survey of nests
One hundred fifty-seven nests of Polistes nimpha were initially found on the selected area plots. A repeat systematic survey of nests has shown that the number of nests recorded decreased substantially by 85.30 % in a short time (the first 3 weeks) (Fig. 2). At the time when pupae and larvae were collected (June 9, 2014), only 17 nests had survived (Fig. 2). Materials for genetic analyses were collected from 15 nests because in the two remaining nests the number of individuals was low. More intense sampling during this phase might diminish substantially or destroy the local population.
The nest destruction was not witnessed, but trace evidence examinations allowed us to conclude that activities of large animals (e.g., foxes), invertebrates (e.g., ants) and/or humans had destroyed the nests. In over 80 % of the cases, the mammals’ activity was the most important predictor of nest mortality. For a large proportion of nests, the reason for their failure is unknown. The degree of destruction varied substantially across sites; only stalks of nests remained (the comb had been damaged), or inhabitants had been eaten, but the nest (comb) had remained untouched (Table 1).
Due to the considerable nest mortality (Fig. 2), only 42 foundresses (of 157 initially identified nests) were marked. Eleven marked foundresses originated from nests sampled for genetic analyses. Based on the mobility behavior of marked foundresses, we can conclude that all these individuals have been observed only on their natal nests. However, not marked, visiting, or usurping (not aggressively behaved) wasps were observed during weekly inspections of localized colonies of P. nimpha on May 8, 2014 and May 14, 2014.
Microsatellite cross-species amplification
High rates of microsatellite amplification were observed. From a total of 13 primer pairs, 12 pairs that amplify without any problems were chosen for genetic analysis. Table S1 shows the characteristics of the pursued and nonamplifiable pair of primers. Eleven microsatellite loci (Pdom 1, 2, 7, 20, 25, 93, 117, 121, 127, 139, 140) were polymorphic, and one locus (Pdom 151) was monomorphic (Table S1). Only eight polymorphic loci had a size variation consistent with the occurrence of strictly stepwise mutations in the repeat array. The remaining primers (Pdom 25, 117, 121) showed more complex patterns of evolution (nonstepwise mutations). These three loci were excluded; thus the truncated set contains data for eight microsatellite loci collected from 59 individuals. Large allele dropout and stuttering were not detected. At the locus Pdom 7, missing data for four individuals probably appeared because of mutations in the primer binding sites.
Genetic diversity and structure within the pooled sample
Standard measures of genetic diversity in P. nimpha population were calculated. The mean PIC score of the microsatellite loci (n = 8) was equal to 0.545, ranging from 0.033 (Pdom 93) to above 0.5 (Pdom 1, 139, 7, 127). The latter four loci are highly polymorphic. The mean number of different alleles per locus was 6.875, ranging from 2 (Pdom 93) to 11 (Pdom 7). The mean expected heterozygosity was 0.5765 (unbiased expected heterozygosity UHe = 0.577), meaning that there is a >57 % chance of being a heterozygote under random mating conditions. The average value of the observed heterozygosity (H o) was slightly higher than Hardy–Weinberg expectations, H o = 0.588. However, no significant deviations from Hardy–Weinberg equilibrium were observed for the alternative hypothesis of heterozygote excess (H1), (P = 0.433 ± SE 0.020). Chi-square tests for individual loci showed a significant deviation (P < 0.05) for Pdom 20 (Chi-square test value using Yates’s correction = 7.622), (Table S2).
To relate observable structure (nests) to the genetic structure of analyzed population, a model-based clustering was employed. Taking genetic information into account, the Bayesian clustering method, based on the individual-level clustering model for unlinked markers, gave the probability of >0.898 of being 10 genetic clusters within the pooled sample of 15 nests (log marginal likelihood of optimal partition = –1025.9824). The inferred six clusters (4, 6–10) were coherent in terms of wasps’ nests (i.e., each cluster contains individuals originated from one nest). The remaining clusters (1–3, 5) were composed of all individuals originated from two nests (clusters 1, 2, and 5) or three nests (cluster 3). The principal coordinate analysis (PCoA) results broadly confirmed the grouping based on BAPS analysis. In the PCoA, the individuals were grouped accordingly, but only 40.97 % of the variation in the input data has been captured by the first three axes (PCoA 1–3), (Figs. 3 and 4). All individuals studied belong to the same generation and based on genetic data all were heterozygous at least at one of analyzed loci. Thus, they represent presumably the same sex (worker-like females), (see Balloux and Lugon-Moulin 2002, Lorenzi 2009).
In the case of organism’s limited dispersal ability, we expect an isolation-by-distance type of population structure, in which genetic similarity is contrarily related to geographical distance calculations (Meirmans and Van Tienderen, 2012). The comparison of linear genetic distances with geographic distances by the Mantel test revealed a significant correlation between genetic and geographic distances (R 2 = 0.0413, P < 0.001); thus, it can be concluded that genetic differences among individuals do increase linearly with geographic distance.
The three metrics of relatedness employed were highly correlated (n = 1711, all r > 0.91). Based on the method-of-moments estimators, the BAPS clusters composed of individuals originated from two or three nests (considered as a group 1, nos. 1–3, 5) expressed significantly lower levels of relatedness coefficients (P < 0.05) than did the second group composed of one-nest clusters (nos. 4, 6–10) (Table S3; Figs. 5 and 6). The ML estimator did not show significant differences between these groups.
Discriminations among plausible relationships (full-sibs, half-sibs, and unrelated) were based on the maximal likelihood. All pairwise comparisons between individuals classified to mixed cluster no. 1 (composed of two nests, nos. 2 and 9, Fig. 1) were classified as full-siblings or parental offspring (here, both categories were considered jointly as full-siblings). However, the mean value of relatedness within this cluster was significantly lower than that within the one-nest clusters (Table S4). In the mixed clusters (nos. 2–3 and 5), the percentage of pairwise comparisons classified as full-siblings ranged from 46.15 to 57.14 %; as half-siblings, from 23.81 to 35.71 %; and as unrelated individuals, from 7.14 to 24.615 % (Fig. 6). In one-nest clusters (nos. 6–10), only full-siblings were found. In one-nest cluster no. 4, the majority of pairwise comparisons were classified as full-sibs, whereas one-sixth were classified as half-siblings; no unrelated individuals were found.
Discussion
Eight loci out of 12 analyzed can be effectively used to genotype individuals of P. nimpha. These most variable perfect loci have the average expected and observed heterozygosities over 0.57, that are comparable but slightly lower than those detected for P. dominula (Henshaw 2000; Henshaw et al. 2011), P. chinensis antennalis (Saigo and Tsuchida 2010), and P. satan (Komatsu et al. 2012).
In the cases of limited number of microsatellite loci (5–20), the method-of-moments estimators is commonly preferred (Csilléry et al. 2006). Nevertheless, different relatedness estimators employed here yielded highly correlated estimates of relatedness between pairs of P. nimpha individuals. Therefore, besides the commonly used, the Queller and Goodnight’s (1989) estimator that was developed for haploid–diploid social Hymenoptera, the maximum-likelihood (ML) estimators (Milligan 2003, Kalinowski and Taper 2006) can be successfully employed in the further studies of social insects.
The Bayesian analysis provided support for the existence of genetic structure in the analyzed population of P. nimpha by partitioning individuals into 10 clusters. This grouping was also broadly confirmed by principal coordinate analyses. The existence of mixed BAPS clusters (i.e., composed of two or three nests) in which only some individuals that originated from different nests are full-sibs and the others are unrelated may indicate three main reproductive tactics in the population of this species: short visits of foundresses, cooperative (pleometrotic) nest foundations, and/or nest usurpation. These tactics in Polistes wasps are hypothesized to have different fitness payoffs over time, depending on environmental shifts (Starks and Fefferman 2006; Seppä et al. 2012).
Pleometrotic nest foundation was described for Polistes species, e.g., European P. dominula (Pardi 1942; Nonacs and Reeve 1995), American P. carolina (L.) (Seppä et al. 2012), neotropical P. versicolor (Olivier) (De Oliveira et al. 2010 and references therein), and P. nimpha (Turillazzi and Cervo 1985). As was hypothesized by Gamboa (1980) and Tibbetts and Reeve (2003), multiple foundresses increase colonies’ productivity and survivorship and make them less likely to be usurped. Nevertheless, this tactic may negatively affect the nest if foundresses are infected by parasites (Hodges et al. 2003 and references therein). To some extent, pleometrotic nest foundation is contradicted by our evidence of marked foundresses of P. nimpha that were seen only on natal (single) nests. Nevertheless, this kind of cooperation cannot be fully excluded due to methodological reasons (marking of wasps was performed shortly after eggs were laid but before offspring emerged). So far, in P. nimpha, pleometrotic nest foundation was detected only at sites where the aggregation of sibling females was possible during the winter (i.e., “in covered and sheltered” places, such as buildings) (Turillazzi and Cervo 1985: 49). The winter destruction of plants and difficulties in the aggregation of females that build nests on this kind of substratum were hypothesized to be main factors for nest foundation by a single foundress (Turillazzi and Cervo 1985). Based on materials, we collected from the nests built on vegetation; the single-foundress colonies comprise only 50 % of detected BAPS clusters. Thus, the causes of pleometrotic nest foundation have yet to be investigated and determined.
Nevertheless, other possibilities also should be considered to interpret population structure of P. nimpha from our genetic data. The possibilities of laying eggs by visiting, nonaggressive wasps in the nests of sibling females or intraspecific usurpation cannot be excluded based on our direct field observations. It should be underlined, however, that in the case of unmarked wasps, there are always difficulties in differentiating a visitor, a joiner, a switcher, an adopter, or a usurper (Nonacs and Reeve 1985). The case of cluster no. 1 being composed of two nests in which full-siblings were found is a prime example of ambiguity because the interpretation could be twofold: eggs were laid by one queen who was fertilized by related males, or eggs were laid by a pair of full sisters. The former phenomenon was discovered for the first time by Seppä et al. (2011) in P. biglumis L.
The results of the comparison of the genetic distances to the geographic distances with the Mantel test suggest that individuals from a particular nest are more genetically related to those inhabiting nearby nests than they are to individuals originating from nests situated in further parts of the study area. Foundresses of the studied nests may be the offspring of one or several closely related queens that returned to their natal sites after hibernation. Cervo and Turillazzi (1985) observed that new colonies of P. nimpha in synanthropic conditions were initiated very closely to the natal nest. It has been shown that the recognition of the natal nest is possible due to the hydrocarbon profile specifics of each Polistes colony (Gamboa 2004; Sumana et al. 2005). Philopatric tendencies in some species of Polistes wasps were observed previously by West-Eberhard (1969), Klahn (1979), Hirose and Yamasaki (1984), Makino et al. (1987) and Cervo and Turillazzi (1985). For example, most colonies of Japanese Polistes wasps are initiated within a distance of 50–80 m (164.5–263 feet) from the natal nest (Hirose and Yamasaki 1984; Makino et al. 1987). Nevertheless, no isolation by distance among populations of P. olivaceus (De Geer) was detected (Uddin and Tsuchida 2011).
However, the tendency of individuals originating from two or three different nests to cluster together can reflect close affinity of some individuals or be a result of stochastic error (Kalinowski 2011). The number of clusters detected by Bayesian clustering algorithms does not always correspond to the number of biologically meaningful populations (groups) in the studied sample (Francois and Durand 2010). Inference of population structure is sensitive to the number of loci scored, the number of populations, the number of individuals per population, the sampling strategy, and the chosen analysis method (e.g., Evanno et al. 2005; Rodriguez-Ramilo et al. 2009; Francois and Durand 2010; Kalinowski 2011; Putman and Carbone 2014). Moreover, as was shown by Frantz et al. (2009), the Bayesian methods employed in BAPS overestimate genetic structure when one or more loci significantly deviate from the Hardy–Weinberg equilibrium and when isolation by distance exhibits high levels (b ≤ −0.01).
Similar to the majority of wildlife studies, this study suffers from several limitations resulting from the small number of available loci for analysis, the relatively small sample size, and the small size of the area from which studied individuals were collected. Moreover, based on data sets analyzed here, isolation-by-distance and a significant deviation from Hardy–Weinberg proportions for one locus were detected. Thus, the presented results should be treated with caution until more data are collected.
A large number of colonies established by paper wasps are relatively soon completely destroyed or substantially damaged by natural enemies such as predators and parasites and by human activity of various kinds (Strassmann 1981; Makino 1983; Cervo and Turillazzi 1985; Rusina 2011) The highest rates of nest mortality, attributable to an external agent, were observed in P. nimpha during the first weeks after nest identification. After nest destruction, foundresses can choose the following options: nesting alone (nest rebuilding), usurping established colonies, or joining other queens (Nonacs and Reeve 1985). Based on our data, no nests rebuilding or joining has been observed (see also Makino 1989). Therefore, dispersing or dying of foundresses has to be considered to explain this observation.
In conclusion, our study demonstrates for the first time a useful panel of microsatellite markers to perform population genetics studies dealing with P. nimpha. There are three main possibilities that come into play to explain our genetic results and direct field observations: cooperative nest foundation, visitation, and/or usurpation events. So far, there is no conclusive evidence to exclude or support any of these possibilities. A philopatric behavior of foundresses is suggested based on genetic data. However, further and more extensive studies in terms of the number of individuals and loci are needed.
References
Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165
Carpenter JM (1996) Distributional checklist of species of the genus (Hymenoptera: Vespidae; Polistinae, Polistini). Am Mus Novit 3188:39
Cervo R (2006) Polistes wasps and their social parasites: an overview. Ann Zool Fennici 43:531–549
Cervo R, Turillazzi S (1985) Associative foundation and nesting sites in Polistes nimpha. Naturwissenschaften 72:48–49
Cervo R, Stemmer C, Castle W, Queller D, Strassman JE (2004) Social parasitism of Polistes dominulus by Polistes nimphus (Hymenoptera, Vespidae). Insect Soc 51:101–108
Corander J, Sirén J, Arjas E (2008) Spatial modelling of genetic population structure. Comput Stat 23:111–129
Csilléry K, Johnson T, Beraldi D, Clutton-Brock T, Coltman D, Hansson B, Spong G, Pemberton J (2006) Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics 173(4):2091–2101
De Oliveira SA, Monteiro de Castro M, Prezoto F (2010) Foundation Pattern, Productivity and Colony Success of the Paper Wasp, Polistes versicolor. J Insect Sci 10:125. doi:10.1673/031.010.12501
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Francois O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour. doi:10.1111/j.1755-0998.2010.02868x
Frantz AC, Cellina S, Krierb A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505. doi:10.1111/j.1365-2664.2008.01606.x
Gamboa GJ (1980) Comparative timing of brood development between multiple- and single-foundress colonies of the paper wasp, Polistes metricus. Ecol Entomol 5:221–225
Gamboa GJ (2004) Kin recognition in eusocial wasps. Ann Zool Fenn 41:789–808
Henshaw MT (2000) Microsatellite loci for the social wasp Polistes dominulus and their application in other Polistine wasps. Mol Ecol 9:2155–2157
Henshaw MT, Toth AL, Young TJ (2011) Development of new microsatellite loci for the genus Polistes from publicly available expressed sequence tag sequences. Insect Soc 58:581–585
Hirose Y, Yamasaki M (1984) Dispersal of females for colony founding in Polistes jadwigae dalla torre (Hymenoptera, Vespidae). Kontyû 52(1):65–71
Hodges AC, Hodges GS, Espelie KE (2003) Parasitoids and parasites of Polistes metricus say (Hymenoptera: Vespidae) in Northeast Georgia. Ann Entomol Soc Am 96(1):61–64
Hughes WO, Ratnieks FL, Oldrovd BP (2008) Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera. J Evol Biol 21(4):1090–1095
Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632
Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv Genet 7:991–995
Klahn JE (1979) Philopatric and nonphilopatric foundress associations in the social wasp Polistes fuscatus. Behav Ecol Sociobiol 5:417–424
Komatsu K, Mateus S, Zucchi R, Nascimento F, Kudo K (2012) Application of microsatellite primers developed for Polistes in the independent-founding wasp Polistes satan Bequaert (Hymenoptera: Vespidae). Neotrop Entomol 41(3):204–206. doi:10.1007/s13744-012-0035-y
Lorenzi M (2009) Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis. Insect Soc 56(4):347–358. doi:10.1007/s00040-009-0030-4
Lorenzi MC, Caldi M, Cervo R (2007) The chemical strategies used by Polistes nimphus social wasp usurpers (Hymenoptera Vespidae). Biol J Linn Soc 91:505–512
Makino S (1983) Biology of Latibulus argiolus (Hymenoptera, Ichneumonidae) a parasitoid of the paper wasp Polistes biglumis (Hymenoptera, Vespidae). Kontyû 51:426–434
Makino S (1989) Usurpation and nest rebuilding in Polistes Riparius: two ways to reproduce after the loss of the original nest (Hymenoptera): Vespidae). Insect Sci 36(2):116–128
Makino S, Sayama K (1991) Comparison of intraspecific nest usurpation between two haplometrotic paper wasp species (Hymenoptera: Vespidae: Polistes). J Ethol 9:121–128
Makino S, Yamane S, Sunose T, Aoki S (1987) Dispersion distance of queens from natal nests in the two haplometric paper wasps Polistes riparius and P. snelleni (Hymenoptera: Vespidae). Res Popul Ecol 29:111–117
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2):209–220
Meirmans PG, Van Tienderen PH (2012) The effects of inheritance in tetraploids on genetic diversity and population divergence. Heredity 110:131–137
Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167
Miyano S, Hasegawa E (1998) Genetic structure of the first brood of workers and mating frequency of queens in a Japanese paper wasp Polistes chinensis antennalis. Ethol Ecol Evol 10:79–85
Miyano S, Shun’ichi Makino S, Yamane S (2010) Polistes formosanus (Hymenoptera: Vespidae) produces males concurrently with females in the first brood on Yoron Island, Southern Japan. Sociobiology 56(1):91–107
Nagamati K Jr, Simokomaki K, Gruber CV, Del Lama MA (2010) Sociogenetic structure of Polistes (Aphanilopterus) versicolor Olivier, 1791 colonies (Hymenoptera, Vespidae, Polistini). Genet. Mol. Biol. 33(4):669–675
Oetting WS, Lee HK, Flanders DJ, Wiesner GL, Sellers TA, King RA (1995) Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers. Genomics 30(3):450–458
Oleksa A, Wiśniowski B (2005) The paper wasp Polistes dominulus (Christ, 1791)—is it really a critically endangered species in Poland (Hymenoptera: Vespidae: Polistinae)? Wiad Entomol 23(3):179–188 [in Polish]
Ono M (1989) Multiple-comb nest foundation by a single inseminated worker of the temperate paper wasp, Polistes snelleni Saussure (Hymenoptera: Vespidae). J Ethol 7(1):57–58
Pardi L (1942) Ricerche sui Polistini. 5. La Poliginia iniziale di Polistes gallicus (L.). Boll Inst Entomol Univ Bologna 14:1–106
Pardi L (1948) Dominance order in Polistes wasps. Physiol Zool 21:1–13
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539. doi:10.1093/bioinformatics/bts460
Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4(22):4399–4428. doi:10.1002/ece3.1305
Queller DC, Goodnight KF (1989) Estimating relatedness using molecular markers. Evolution 43:258–275
Raymond M, Rousset F (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419
Rodriguez-Ramilo ST, Toro MA, Fernandez J (2009) Assessing population genetic structure via the maximization of genetic distance. Genet Sel Evol 41:49. doi:10.1186/1297-9686-41-49
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8(1):103–106
Rusina LYu (2011) Some Aspects of Interrelations between Ants (Hymenoptera, Formicidae) and Polistinae Wasps (Hymenoptera, Vespidae). Entomol Rev 91(2):241–252
Saigo T, Tsuchida K (2010) Nine newly designed polymorphic microsatellite loci for the Japanese paper wasp, Polistes chinensis antennalis (Hymenoptera: Vespidae). Appl Entomol Zool 45(4):575–577
Sayama K, Takahashi J (2005) Mating structure and genetic relatedness among gynes in the primitively eusocial wasp Polistes snelleni (Hymenoptera: Vespidae). Entomol Sci 8:27–31
Seppä P, Fogelqvist J, Gyllenstrand N, Lorenzi MC (2011) Colony kin structure and breeding patterns in the social wasp, Polistes biglumis. Insect Soc 58:345–355
Seppä P, Queller DC, Strassmann JE (2012) Why wasp foundresses change nests: relatedness, dominance, and nest quality. PLoS One 7(9):e45386
Starks PT, Fefferman NH (2006) Polistes nest founding behavior: a model for the selective maintenance of alternative behavioral phenotypes. Ann Zool Fennici 43:456–467
Strassmann JE (1981) Parasitoids, predators, and group size in the paper wasp, Polistes exclamans. Ecology 62(5):1225–1233
Strassmann JE, Barefield K, Solis CR, Hughes CR, Queller DC (1997) Trinucleotide microsatellite loci for a social wasp, Polistes. Mol Ecol 6:97–100
Sumana A, Liebert AE, Berry AS, Switz GT, Orians CM, Starks PT (2005) Nest hydrocarbons as cues for philopatry in a paper wasp. Ethology 111:469–477
Tibbetts EA, Reeve HK (2003) Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns. Behav Ecol 14:510–514
Tsuchida K, Kudo K, Ishiguro N (2014) Genetic structure of an introduced paper wasp, Polistes chinensis antennalis (Hymenoptera, Vespidae) in New Zealand. Mol Ecol 23(16):4018–4034
Turillazzi S, Cervo R (1982) Territorial behaviour in males of Polistes nimpha (Christ) (Hymenoptera, Vespidae). Z Tierpsychologie 58:174–180
Uddin MM, Tsuchida K (2011) Genetic population structure of the paper wasp Polistes olivaceus (Hymenoptera: Vespidae) in Bangladesh. Popul Ecol. doi:10.1007/s10144-011-0290-5
Van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256
Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
Wang J (2011) Coancestry. A program for simulating estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11(1):141–145
Weir BS (1996) Disequilibrium. Genetic data analysis II: methods for discrete population genetic data. Sinaur Associates, Sunderland, pp 91–139
Weir BS, Anderson AD, Hepler AB (2006) Genetic relatedness analysis: modern data and new challenges. Nat Rev Genet 7:771–780
West-Eberhard MJ (1969) The social biology of polistine wasps. Misc Publ Mus Zool Univ Michigan 140:1–101
Wilson EO (1979) Społeczeństwa owadów. Państwowe Wydawnictwo Naukowe, Warszawa (in Polish)
Acknowledgments
The research was supported by the Dean of Faculty of Biology at Adam Mickiewicz University in Poznań, Poland, Grant No. GDWB-06/2013 to Krzysztof B. Kozyra.
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Kozyra, K.B., Melosik, I. & Baraniak, E. Genetic diversity and population structure of Polistes nimpha based on DNA microsatellite markers. Insect. Soc. 62, 423–432 (2015). https://doi.org/10.1007/s00040-015-0421-7
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DOI: https://doi.org/10.1007/s00040-015-0421-7