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Open Access Research article

Shape differences rather than size differences between castes in the Neotropical swarm-founding wasp Metapolybia docilis (Hymenoptera: Vespidae, Epiponini)

Mário V Baio1, Fernando B Noll12* and Ronaldo Zucchi1

Author Affiliations

1 Departamento de Biologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901-Riberão Preto (SP), Brazil

2 Museum of Biological Diversity, Department of Entomology, The Ohio State University, 1315 Kinnear Road, Columbus, OH 43212; USA

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BMC Evolutionary Biology 2003, 3:10  doi:10.1186/1471-2148-3-10


The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2148/3/10


Received:16 January 2003
Accepted:13 May 2003
Published:13 May 2003

© 2003 Baio et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

Abstract

Background

Swarm-founding epiponine wasps are an intriguing group of social insects in which colonies are polygynic (several queens share reproduction) and differentiation between castes is often not obvious. However, caste differences in some may be more pronounced in later phases of the colony cycle.

Results

Using morphometric analyses and multivariate statistics, it was found that caste differences in Metapolybia docilis are slight but more distinct in latter stages of the colony cycle.

Conclusions

Because differences in body parts are so slight, it is proposed that such variation may be due to differential growth rates of body parts rather than to queens being larger in size, similar to other previously observed epiponines.

Background

Polistine wasps in the tribe Epiponini are remarkable for their polygyny, swarm-founding habits, and reputed slight differentiation between castes. Although the overall features of epiponines are well-documented and discussed [1-3], many sociobiological details remain obscure. For example, for decades, swarm-founding polistines have been considered permanently polygynous, even though monogyny has been detected in some species [1,4,5]. An explanation was offered by [6], who showed that Metapolybia aztecoides alternates between polygyny and oligogyny and, eventually monogyny in the course of its life cycle. This cyclical oligogyny [6] seems to be important in the maintenance of high genetic relatedness in epiponine wasps [7-9]. In fact, new queens are produced with just one queen in the nest [10] in some species.

Preliminary overall studies [1,4] demonstrated a wide range of queen-worker dimorphism among different taxa in the Epiponini. Three different forms of queen-worker distinction were recognized [1], but, recently, five forms of caste differentiation due to the influence of the colony cycle were recognized [11]. They are: 1, the absence of morphological differences between queens and workers during the entire colony cycle (Parachartergus smithii [12], Pseudopolybia vespiceps [13], Chartergellus communis [14], Brachygastra lecheguana [15]); 2, the absence of morphological differences between castes, with some young females developing ovaries in only some phases of the colony cycle (Synoeca cyanea [16]); 3, morphological discontinuities between castes related to variation during the colony cycle, with non-inseminated laying females present during the entire colony cycle (Protopolybia exigua and P. sedula [11]); 4, caste differences increase during the colony cycle with non-inseminated laying females occurring only some phases of the colony cycle(Chartergus globiventris [11], Polybia scutellaris, P. occidentalis, and P. paulista [17], Protonectarina sylveirae [11], Epipona guerini [18]) and; 5, queens always distinct from workers, with no variation in this pattern occuring during the colony cycle (Agelaia areata [19], A. vicina [20,21], A. pallipes and A. multipicta [22], Apoica flavissima [23] and A. pallens [24], Polybia dimidiata [25]).

Even though Metapolybia may be considered a model genus for studies related to colony population structure in epiponines, just a few studies (taxonomy – [26], ovary development – [27], colony composition, including caste differences [28] and nest construction – [29]) have been performed on this taxon since [6], despite the increase in knowledge of this tribe. This paper examines caste differences and other ecological aspects of Metapolybia docilis.

Results

Nests and related aspects

Colonies under investigation were assigned to one of 4 stages, after [17] (Table 1): (a) pre-emergence of workers, in which no adult offspring had been produced (one colony); (b) emergence of workers, with different-aged brood and at least one adult generation (one colony); and (c) male producing (one colony). Also, two other colonies were migrating for a new location. This fourth stage was defined as (d) swarm or absconding (two colonies). Even though these two forms of swarm are difficult to distinguish, behavioral observations (unpublished data) indicated that only part of the population migrated to a new nest in the swarm colony. In addition, swarming queens were exclusively younger females (see below) suggesting production of sexuals in the mother nest. The absconding colony represents the migration of a whole colony after some disturbance once the nest was damaged. In addition all queens were old (see below) evidencing that this colony was not producing new queens, representing the end of a cycle.

Table 1. Number of combs, brood production, and colony population in the analyzed colonies of Metapolybia docilis. Percentage in parentheses.

Females' ovary condition, insemination and their relative age

Two types of ovarian development were recognized as type A, with filamentous ovarioles bearing no visible or slightly developed oocytes, and type B, with well developed and longer ovarioles, each one bearing from two to several mature oocytes. Since only type B females contained sperm in the spermatheca, females with type A and B ovarian development can be characterized as workers and queens, respectively.

According to our data, the colony cycle in Metapolybia docilis is characterized by great age variation (Figure 1). In the pre-emergence colony both workers and queens varied substantially in age. In worker-producing and male-producing colonies most workers were younger and most queens were older. In the absconding colony, workers varied in age, but the single queen was old (black pattern). In the swarm colony, queens and workers were young and old individuals, respectively, without intermediate age.

thumbnailFigure 1. Frequency of queens (White bars) and workers (dark bars) according to the color patterns of the transverse apodeme from the 4th gastral sternite in Metapolybia docilis in different analyzed colonies. LY – light yellow, LB – light brown, DB – dark brown, B – black.

Morphological differences

Mean differences of 10 measured characters were tested in workers and queens by Bonferroni t-test (Table 2). In all analyzed colonies queens were hardly distinct from workers. Univariate statistics showed that just a few characters for each colony were different among queens and workers (Table 2) in all colonies. Except for MTL in a worker-producing colony, all significant differences showed queens slightly larger than workers. Using the characters with significant differences in univariate statistics, covariance analysis (ANCOVA: Table 2) showed statistically significant values in all these characters except for T1L in the pre-emergence colony, demonstrating that these characters differed in size and body proportions. ANCOVA was not tested in the absconding colony due to the presence of only one queen.

Table 2. Queen and worker means (in mm), Bonferroni t-test and ANCOVA analyses for each morphometrical variable in Metapolybia docilis.

Discriminant function analysis (Table 3) showed also that only a few characters used in the model resulted in significant p-values. Wilk's Lambda values ranged from 0.64 to 0.8 (Table 10) in pre-emergence and worker-producing colonies and from 0.13 to 0.75 (one variable only) in male-producing and swarm colonies. This indicates that in the former some individual characters were not good enough to discriminate castes, and caste differences could be determined only in association with these characters, which demonstrates low differentiation between castes (Fig. 2). In the latter, however, some characters appear to have a better power of discrimination (Fig. 2). Such differences suggest that variation during the colony cycle may occur as in other epiponines [11,17]. In fact, comparing actual groups with predicted groups through discriminant analysis (Table 3), it is evident that queens form more distinct groups in the later stages of the colony cycle. These results emphasize how queens, apart from being hardly distinguishable by size, exhibit some differences that are perhaps more related to shape than size.

thumbnailFigure 2. Plots (in mm) of alitrunk length (AL) versus basal height tergum II (T2H) in five colonies of Metapolybia docilis. Queens = black squares; Workers = white circles. Each ellipse encompasses 95% of the variation found in each group. A – discrimination between all queens and workers of Metapolybia docilis using the log-log plots.

Table 3. Discriminant morphometric variables between queens and workers in Metapolybia docilis based on discriminant function analyses using the stepwise procedure and classification results for group comparisons through discriminant analysis. Original data are based on mm.

Discussion

In Metapolybia, castes are hardly detectable by external morphology [1,28], and they are apparently determined by disputes among adults rather than by larval manipulation [6,30]. For this reason, young females have their ovaries suppressed in queen-right colonies, and only in orphanage young females develop their ovaries and become queens [6]. In our study, Metapolybia docilis exhibits slight differentiation between queens and workers, at least in the early stages of nest development, as compared to other taxa such as Agelaia spp. (A. flavipennis [31]; A. areata, [19]; A. pallipes and A. multipicta [22]; A. vicina [20,21]) that have a clear-cut caste differentiation. Also, the clear physiological distinction found between queen and worker ovaries (Fig. 2) suggest strong control of reproduction.

Group comparisons (Table 3) showed queens and workers as unique, well-defined groups, in the latter stages of the colony cycle. In addition, Wilks' Lambda values were relatively low for such colonies (Table 3), demonstrating that, in these colonies, castes can be relatively well-recognized by morphology in the later stages of the colony cycle. Such a pattern seems to be widespread for the Epiponini [11,17], and it is suggested that the increase in castes differences is probably due to the elimination of the smaller queens. The fact that queens in the later stages of the colony cycle are slightly more distinct from those found in early stages suggest that the phenomenon of queen-selection [6] during the colony cycle may have a morphological component similar to other species previously studied [11,17]. In Synoeca cyanea [16], a similar pattern was identified. However, intermediate females were found in some colonies and differences between castes were always absent.

Differently from other species with increasing caste differences according to colony cycle, in M. docilis, size differences are very slight. Based on the plots of figure 2, castes are always intersecting each other, and in figure 2A, the growth rates, represented by different slopes detected by ANCOVA analyses (Table 2), are different between castes. Such results indicate that queens and workers differ more in shape than in size. Shape differences have been previously detected for Apoica pallens [24] but, in this case, it was accompanied by size differences, as in other species, such as Epipona guerini [18] and Pseudopolybia difficilis [32]. According to [24] it is possible that the first step of caste evolution in epiponines may be related to changes in body proportions rather than in size due to an ontogenetic reprogramming in the growth parameters (see also [33]). Thus, the almost absence of queen-worker size differences in Metapolybia illustrates how complex castes in epiponines is.

Low morphological differentiation accompanied by high physiological distinction was suggested for Synoeca and Metapolybia [6,30]. In these cases, only certain females that are already mated become queens. During cyclical oligogyny, a low number of queens would signal that new females would "take a chance" to become new queens. After queen repopulation, orphanage behaviors cease, and workers use aggressive behaviors to inhibit other new females from becoming queens. In this case, non-inseminated ovarian-developed females, common in the some epiponines [11] are completely suppressed during the entire colony cycle due to worker policing as suggested by [11]. In fact, queens' age (Fig. 1) reinforces such assumption, once pre-emergence colonies initiate with differently aged queens, and only older queens are found in worker-producing and male-producing colonies. In swarming colonies, the queen population is composed either of very young or very old individuals, suggesting that new reproductive are produced only during discrete windows of time.

The fact we found some distinction between castes would not reject the possibility of some young individuals (potential workers) may try to become queens [6,30]. Their options would be two-fold: they could lead the colony until a new queen repopulation occurs, or they could compete with those true queens during the early stages of the colony cycle. However, they would probably be removed from the colony as the cycle progresses [11].

Conclusions

As stated by [4] and [31], because epiponines frequently migrate, development of true castes would not be advantageous. This assertion may be correct in part, once castes are hard to detect. However, differently from the other "highly eusocial insects" (bees, ants, termites and vespine wasps) which bear pronounced size dimorphism, caste differences in epiponines evolved in such a way that imperceptible size differences are expected in most species, probably due to reprogramming of growth parameters [24]. The pattern of caste differences found in Metapolybia docilis supports this hypothesis.

Methods

Five colonies of Metapolybia docilis used in this work were collected at nightfall. They were collected into a plastic bag containing ether-moistened cotton balls. Populations were fixed in Dietrich's solution and then kept in 70 % ethanol for dissection. In order to detect morphological differences between the castes, the following 10 external body parts were measured for each specimen under a binocular microscope; head width (HW), head length (HL), minimum interorbital distance (IDm), pronotum width (PW), mesoscutellum length (MTL), alitrunk length (AL), length of gastral tergite I (T1L), basal width of gastral tergite II (T2BW), height of T2 (T2H) and partial length of the forewing (WL) (see also Fig. 2 in [23] more details about these measurements). We examined ovarian conditions by dissecting all individuals under a stereomicroscope. In order to analyze insemination, the spermatheca was removed and put on a slide in a 1:1 solution of glycerin and alcohol (70%). The presence of sperm cells was detected by using a compound microscope. Numerical data were statistically analyzed in relation to the ovarian and spermathecal states.

Before statistical analysis, data were log transformed. Means and standard deviations were calculated from the ten morphological measurements. The Bonferroni t test was used for mean comparisons. The contribution of each variable to caste discrimination was examined using stepwise discriminant function analysis [34]. In this method, variables are successively added to the model based on the higher F to enter values; variable addition ceases when the F-ratio is no longer significant. Wilks' Lambda values were used to infer the individual contribution of each variable to the model. ANCOVA was used with alitrunk length (AL) as a covariate based on its efficiency in previous publications [18,24,32].

In order to assess the age of females, progressive pigmentation of the transverse apodeme was analyzed. The patterns used here were those that, according to [4,35] indicate a progressive increase in age. They were: LY (light yellow) for the youngest individuals, LB (light brown), DB (dark brown) and B (black) for the oldest individuals.

Authors' contributions

MVB participated in morphometric analyses, females' dissections. FBN and RZ participated in the design of the study, performed the statistical analysis and wrote the manuscript. All authors read and approved the final manuscript.

Acknowledgments

The authors acknowledge the financial support by FAPESP proc. 97/13204-9 and 01/02491-4. Special thanks to Sidnei Mateus for helping in field collections and Kurt M. Pickett (The Ohio State University) for corrections on the manuscript and important suggestions.

References

  1. Richards OW: The social wasps of the Americas excluding the Vespinae.

    London. British Museum (Natural History) 1978. OpenURL

  2. Carpenter JM: Phylogenetic relationships and the origin of social behavior in the Vespidae. In The social biology of wasps. Edited by Ross KG, Matthews RW. Cornell University Press, Ithaca, New York; 1991:7-32. OpenURL

  3. Jeanne RL: The swarm-founding Vespidae. In The social biology of wasps. Edited by Ross KG, Matthews RW. Cornell University Press, Ithaca, New York; 1991:191-231. OpenURL

  4. Richards OW, Richards MJ: Observations on the social wasps of South America (Hymenoptera, Vespidae).

    Trans Roy Entomol Soc London 1951, 102:1-170. OpenURL

  5. Richards OW: The biology of the social wasps (Hymenoptera, Vespidae).

    Biol Rev 1971, 46:483-528. OpenURL

  6. West-Eberhard MJ: Temporary queens in Metapolybia wasps: non-reproductive helpers without altruism?

    Science 1978, 200:441-443. OpenURL

  7. Queller DC, Hughes CR, Strassmann JE: Genetic relatedness in colonies of tropical wasps with multiple queens.

    Science 1988, 242:1155-1157. OpenURL

  8. Queller DC, Negrón-Stomayor JA, Hughes CR, Strassmann JE: Queen number and genetic relatedness in a neotropical wasp, Polybia occidentalis.

    Behav Ecol 1993, 4:7-13. OpenURL

  9. Hughes CR, Queller DC, Negrón-Sotomayor JA, Strassmann JE, Solis C, Gastreich KR: The maintenance of high genetic relatedness in multi-queen colonies of social wasps. In Queen number and sociality in insects. Edited by Keller L. Oxford University press, New York; 1993. OpenURL

  10. Strassmann JE, Goodnight KF, Kihger CJ, Queller DC: The genetic structure of swarms and the timing of their production in the queen cycles of neotropical wasps.

    Molecular Ecology 1998, 7:709-718. Publisher Full Text OpenURL

  11. Noll FB, Zucchi R: Caste and influence of the colony cycle in swarm-founding polistine wasps (Hymenoptera, Vespidae, Epiponini).

    Insectes Sociaux 2002, 49:62-74. Publisher Full Text OpenURL

  12. Mateus S, Noll FB, Zucchi R: Morphological caste differences in neotropical swarm-founding polistinae wasps: Parachartergus smithii (Hymenoptera: Vespidae).

    J New York Entomol Soc 1997, 105:129-139. OpenURL

  13. Shima SN, Noll FB, Zucchi R, Yamane S: Morphological caste differences in the Neotropical swarm-founding polistine Wasps IV. Pseudopolybia vespiceps, with preliminary considerations on the role of intermediate females in social organization of the Epiponini (Hymenoptera, Vespidae).

    J Hym Res 1998, 7:280-295. OpenURL

  14. Mateus S, Noll FB, Zucchi R: Caste differences and related bionomic aspects of Chartergellus communis, a neotropical swarm-founding polistine wasp (Hymenoptera: Vespidae: Polistinae: Epiponini).

    J New York Entomol Soc 1999, 107:390-405. OpenURL

  15. Shima SN, Noll FB, Zucchi R: Morphological caste differences in the neotropical swarm-founding polistine wasp, Brachygastra lecheguana (Hymenoptera: Vespidae, Polistinae, Epiponini).

    Sociobiology 2000, 36:41-52. OpenURL

  16. Noda SCM, Shima SN, Noll FB: Morphological and physiological caste differences in Synoeca cyanea (Hymenoptera, Vespidae, Epiponini) according to the ontogenetic development of the colonies.

    Sociobiology 2003, 41:547-570. OpenURL

  17. Noll FB, Zucchi R: Increasing caste differences related to life cycle progression in some neotropical swarm-founding polygynic wasps (Hymenoptera: Vespidae: Epiponini).

    Ethol Ecol Evol 2000, 12:43-65. OpenURL

  18. Hunt JH, Schmidt DK, Mulkey SS, Williams MA: Caste dimorphism in Epipona guerini (Hymenoptera: Vespidae): Further evidence for larval determination.

    J Kansas Entomol Soc 1996, 69:362-369. OpenURL

  19. Jeanne RL, Fagen R: Polymorphism in Stelopolybia areata (Hymenoptera, Vespidae).

    Psyche 1974, 81:155-166. OpenURL

  20. Sakagami SF, Zucchi R, Yamane S, Noll FB, Camargo JMF: Morphological caste differences in Agelaia vicina, the neotropical swarm-founding Polistinae wasp with the largest colony size among social wasps (Hymenoptera, Vespidae).

    Sociobiology 1996, 28:207-223. OpenURL

  21. Baio MV, Noll FB, Zucchi R, Simões D: Non-allometric caste differences in Agelaia vicina (Hymenoptera, Vespidae, Epiponini).

    Sociobiology 1998, 32:465-476. OpenURL

  22. Noll FB, Simões D, Zucchi R: Morphological caste differences in the neotropical swarm-founding Polistine wasps: Agelaia m. multipicta and A. p. pallipes (Hymenoptera Vespidae).

    Ethology Ecology & Evolution 1997, 9:361-372. OpenURL

  23. Shima SN, Yamane S, Zucchi R: Morphological Caste Differences in Some Neotropical Swarm-founding Polistinae Wasps I. Apoica flavissima (Hymenoptera, Vespidae).

    Jap J Ent 1994, 62:811-822. OpenURL

  24. Jeanne RL, Graf CA, Yandell BS: Non-Size-Based morphological castes in a social insect.

    Naturwissenschaften 1995, 82:296-298. Publisher Full Text OpenURL

  25. Shima SN, Yamane S, Zucchi R: Morphological Caste Differences in Some Neotropical Swarm-founding Polistinae Wasps II. Polybia dimidiata (Hymenoptera, Vespidae).

    Jpn J Ent 1995, 64:131-144. OpenURL

  26. Smethurst ME, Carpenter JM: A new species of Metapolybia ducke from Central America (Hymenoptera: Vespidae; Polistinae).

    J New York Ent Soc 1998, 105:180-185. OpenURL

  27. Itô Y, Yamauchi K, Tsuchida K: Reproductive condition of females in some swarm-founding wasps in Panama, as compared with some independent-founding species (Hymenoptera: Vespidae).

    Sociobiology 1997, 29:269-276. OpenURL

  28. Carpenter JM, Ross KG: Colony composition in four species of Polistinae from Suriname, with a description of the larva of Brachygastra scutellaris (Hymenoptera, Vespidae).

    Psyche 1984, 91:237-250. OpenURL

  29. Karsai I, Wenzel JW: Organization and regulation of nest construction behavior in Metapolybia wasps.

    J Ins Behav 2000, 13:111-140. Publisher Full Text OpenURL

  30. West-Eberhard MJ: Intragroup selection and evolution of insect societies. In In Natural selection and social behavior. Edited by Alexander RD, Tinkle DW. Chiron Press, New York; 2000:3-17. OpenURL

  31. Evans H, West-Eberhard MJ: The wasps.

    Univ Michigan, Ann Arbor 1970. OpenURL

  32. Jeanne RL: Non-allometric queen-worker dimorphism in Pseudopolybia difficilis (Hymenoptera: Vespidae).

    J Kansas Entomol Soc 1996, 69:370-374. OpenURL

  33. Wheeler DE: The development basis of worker castes polymorphism in ants.

    Am Nat 1991, 138:1218-1238. Publisher Full Text OpenURL

  34. Rao CR: Linear statistical inference.

    John Willey and Sons, New York 1973. OpenURL

  35. Forsyth A: Studies on the behavioral ecology of polygynous social wasps.

    Doctoral Dissertation, Harvard University, Cambridge 1978. OpenURL