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Castes in the neotropical social wasp Leipomeles dorsata (Fabricius) (Hymenoptera: Vespidae): a window for workers achieving a new status in the colony

Abstract

Morphometric studies performed in several species of Neotropical social wasps from the tribe Epiponini showed that in some species there are marked differences between castes, while other species present highly distinct castes with differences only in ovarian development. This work analyzed females from six colonies of the social wasp Leipomeles dorsata (Fabricius) in which queens (egglayers) and workers showed differences in ovarian development and coloration. We propose that wasps with developed ovaries (egglayers) and coloration similar to those of workers are possibly intermediates that obtained the status of queens in the colony.

Epiponini; caste difference; multivariate analysis


ECOLOGY, BEHAVIOR AND BIONOMICS

Castes in the neotropical social wasp Leipomeles dorsata (Fabricius) (Hymenoptera: Vespidae): a window for workers achieving a new status in the colony

Fernando B NollI; Bruno GomesI; Alexandre C O LimaII; Sidnei MateusII; John W WenzelIII

ILab de Vespas Sociais, Depto Zoologia e Botânica, Instituto de Biociências, Letras e Ciências Exatas, Univ Estadual Paulista Júlio de Mesquita Filho, Rua Cristóvão Colombo 2265, 15054-000, São José do Rio Preto, SP, Brasil; noll@ibilce.unesp.br, biologia_unesp@yahoo.com.br

IIDepto Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, Av Bandeirantes 3900, 140140-901 Ribeirão Preto, SP, Brasil; alecolima@hotmail.com, sidneim@ffclrp.usp.br

IIIDepartment of Entomology, The Ohio State University, 1315, Kinnear Road, Columbus, Ohio, USA; wenzel.12@osu.edu

ABSTRACT

Morphometric studies performed in several species of Neotropical social wasps from the tribe Epiponini showed that in some species there are marked differences between castes, while other species present highly distinct castes with differences only in ovarian development. This work analyzed females from six colonies of the social wasp Leipomeles dorsata (Fabricius) in which queens (egglayers) and workers showed differences in ovarian development and coloration. We propose that wasps with developed ovaries (egglayers) and coloration similar to those of workers are possibly intermediates that obtained the status of queens in the colony.

Key words: Epiponini, caste difference, multivariate analysis

Theories for the evolution of eusociality (Hamilton 1964a,b, Alexander 1974) have greatly directed studies and discussions toward the potential contribution of females in the gene pool of the next generation. Worker sterility is now a paradigm (West-Eberhard 1975, Anderson 1984, Brockman 1984). However, it is often only partial, and workers often combine the usual helper repertory with some kind of reproduction-related activities (Bourke 1988). In highly eusocial insects, striking examples are found in stingless bees (Zucchi 1993) and Neotropical swarm-founding wasps (Noll et al 2004).

In social wasps (Vespidae), the Epiponini is a very intriguing neotropical tribe of Polistinae (Carpenter 2004). The whole tribe is highly eusocial and polygynic (i.e., several egglayers commonly reproduce simultaneously on the same nest). Their societies are complex (Bourke 1998) because all reproduce by swarms (Jeanne 1991) and division of labor is highly specialized (O´Donnell 1998). Castes in this tribe challenge standard definitions. As expected for highly eusocial insects, pre-imaginal caste determination has been reported in at least five genera (Noll et al 2004). However, in at least six genera (Noll et al 2004), reproductive females resemble non-reproductives in terms of morphology, and castes also lack physiological discontinuities. In these cases, castes are flexible and determined by disputes among adults rather than by larval manipulation (West-Eberhard 1981, Mateus et al 2004, Noll & Wenzel 2008).

Leipomeles is part of a clade that bears slight morphological caste differences. Leipomeles dorsata (Fabricius) are very shy, and when disturbed, females hardly demonstrate aggressiveness (Richards 1978). According to Noll et al (2004), egglayers and workers of Metapolybia (Ducke) and Synoeca (L.) lack morphological differences during the colonial cycle and females are able to develop their ovaries only in some phases of the colonial cycle. In this paper, we analyzed in detail the morphology and physiology of castes in L. dorsata using several colonies and found that some workers may reach the egglayer status, leading reproduction in the absence of a regular egglayer.

Material and Methods

Six colonies of L. dorsata, collected in Presidente Figueiredo, AM, Brazil (01° 49' 596´´ S, 060° 12' 078´´ W) were collected with plastic bags at nightfall or in early morning and all adult wasps from each colony were preserved in 95% ethanol immediately after collection.

Caste was determined by examination of the ovaries and insemination. In order to verify insemination, the spermatheca was removed and analyzed. The presence of sperm cells was detected under a microscope. Groups for analysis were defined based on ovarian development and insemination. egglayers were defined as inseminated females, intermediates as females with some ovarian development, and workers as females without ovarian development. Intermediates and workers were uninseminated females. However, it is important to point out that the definition of these groups is not an indication that they are castes or sub-castes. Hereafter, intermediates and workers will be treated simply as workers.

In order to estimate the relative age of adult wasps by noting the progressive pigmentation of the transverse apodeme across the hidden base of each sternum, all measured individuals were analyzed under a stereomicroscope. Females were classified as young (without or with incipient pigmentation) (Fig 1a), middle-aged (light pigmentation) (Fig 1b) and old (dark pigmentation) (Fig 1c) following Richards (1971) and West-Eberhard (1973).



All individuals of each colony were used for morphometric analysis. Measurements were taken from eight morphometric variables in each female (Fig 2). Measurements were taken using a stereomicroscope equipped with a video camera linked to a computer. Egglayer and worker differences for each variable were tested using the Bonferroni-corrected t-test after ANOVA analyses. A stepwise discriminant analysis was used to identify the most significant contributors for caste distinction. Later, the most discriminant characters were plotted for caste discrimination. Wilks' Lambda values were used to infer the individual contribution of each variable to the model. In order to check the efficiency of the test, a classification matrix test was used to check the number and percent of correctly classified cases in each group.


Results

Physiological differences and females' age. Four patterns of ovarian development were identified in the studied colonies ranging from undeveloped to fully developed (Table 1): 1 filamentous ovarioles bearing no visible oocytes or slightly developed oocytes, 2 large immature oocytes located at the base of the ovary, 3 well-developed oocytes and at least one mature oocyte, 4 well-developed ovarioles with several mature oocytes. Patterns 1, 3 and 4 were found in all colonies, except colony 2 that lacked pattern 3 and colony 40 that lacked pattern 4. Pattern 2 was found only in colonies 27 and 31. Insemination was found only in females having patterns 3 and 4, and apparently, they are related to two color patterns found in egglayers (see below).

Females were classified in three different relative ages: young, middle-age and old (Fig 3). All colonies show individuals with different ages except in colony 27, that all egglayers and workers were old, and colony 40 all egglayers and workers were young individuals (Fig 3). The observed differences in the age of individuals certainly indicates different phases of the colonial cycle (Mateus et al 2004).


Morphological differences. Morphological studies indicated low distinction based on size (Table 2). Except in colonies 2 and 26, no statistical differences were found between egglayers and workers (Table 3). Egglayers from colony 2 were larger than workers, but the opposite was observed in colony 26 (Table 2). Multivariate analysis indicated that the differences found were very low (Tables 2 and 3) as observed by the high Wilks' lambda values (Table 2), which ranged from 0.71 to 0.99 (in a scale that varies from 0 to 1 where 0 indicates total discrimination, and 1 indicates no discrimination). The same result was confirmed after the classification test (Table 4) in which only colony 2 classified egglayers correctly in a 75% level.

Color differences. Size was not a good discriminator, but color seemed to give interesting clues for the social organization of L. dorsata (Fig 4). Workers and intermediates presented a pale color, but with several spots that varied from chestnut to dark brown. The color patterns in 52% of the egglayers were similar to those found in workers and intermediates. However, 42% of the egglayers were mostly yellow in their heads, thorax and abdomen (Fig 4). These differences were not related to age, because all yellow egglayers were old; but brown egglayers may be both young and old. Interestingly, yellow egglayers presented larger ovaries (pattern 4, see above) and darker egglayers smaller ovaries (pattern 3, see above).


Discussion

In our study, L. dorsata only presented slightly morphologic differentiation between egglayers and workers. Also, there is a physiological distinction found between egglayers and worker ovaries, except for the presence of a few females with ovarian development (but, see below), that may suggest strong control of reproduction. Group comparisons showed that egglayers are not a well-defined group based on size. In addition, Wilks' Lambda values were high demonstrating that in these colonies caste recognition is hardly done based on adult wasp morphology. In fact, castes morphological traits are always intersecting each other.

Even with slight morphologic differences, some egglayers of L. dorsata can be clearly separated by color as in Protonectarina sylveirae (Saussure) (Shima et al 1996) and other species of Epiponini (Richards 1978). Two patterns of color were found in L. dorsata egglayers, one that is yellow and bearing longer ovaries and other resembling workers in color and with smaller ovaries when compared to yellow egglayers. Because this color difference is so striking, we suggest that brown egglayers are, in fact, former workers that reached egglayer status (Mateus et al 2004).

As observed in Synoeca and Metapolybia (West-Eberhard 1978, 1981), young females, when orphaned by loss of the egglayers would lead the colony until new egglayers are produced or they may compete with those true egglayers during the early stages of the colony cycle. Our data support both hypotheses, because we found colonies with both kinds of egglayers. In only one colony, however, yellow egglayers were absent and only two brown egglayers were found. Because these females always bear small ovaries, it is possible that they may function as replacements, leading the colony to a new sexual production. Another interesting fact is that in the presence of a very low number of yellow egglayers, there are more brown egglayers and some intermediates (that might simply be brown, but uninseminated egglayers). On the other hand, in the presence of more yellow egglayers there are a few brown egglayers and no intermediates.

Low morphological differentiation accompanied by high physiological distinction was found in Asteloeca (Raw), Synoeca and Metapolybia (Baio et al 2003, Noll et al 2004). During cyclical oligogyny, a low number of egglayers would signal new females to become new egglayers (West-Eberhard 1978, Strassmann et al 1991). After egglayers re-population, orphanage behaviors cease and workers use aggressive behaviors to inhibit other new females from becoming egglayers (Baio et al 2003). In fact, we found only worker-like egglayers in colony 40, reinforcing the assumption that new reproductives are produced only during discrete windows of time; however, young workers would be some kind of "backup" egglayers. Even though this may sound odd, a similar strategy is found in the Neotropical bumble bee Bombus atratus (Silva-Matos & Garófalo 1996), in which queens may be killed by workers and some inseminated workers assume reproduction in the colony until the production of new reproductives.

Acknowledgments

The specimens were collected under the permits from IBAMA authorization (10739-1).The authors acknowledge the financial support by FAPESP (2005/00087-2; 2007/08633-1).

Received 27/XI/08.

Accepted 16/I/09.

Edited by Kleber Del Claro UFU

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Publication Dates

  • Publication in this collection
    14 Sept 2010
  • Date of issue
    Aug 2010

History

  • Received
    27 Nov 2008
  • Accepted
    16 Jan 2009
Sociedade Entomológica do Brasil Sociedade Entomológica do Brasil, R. Harry Prochet, 55, 86047-040 Londrina PR Brasil, Tel.: (55 43) 3342 3987 - Londrina - PR - Brazil
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