Benefits and Costs of Secondary Polygyny in the Dampwood Termite

POPULATION ECOLOGY Beneﬁts and Costs of Secondary Polygyny in the Dampwood Termite Zootermopsis angusticollis

1 2 3 COLIN S. BRENT, JAMES F. A. TRANIELLO, AND EDWARD L. VARGO

Environ. Entomol. 37(4): 883Ð888 (2008) ABSTRACT Newly molted female neotenic reproductives of the dampwood termite Zootermopsis angusticollis Hagen were allowed to mature in the presence of a neotenic male, a Þxed number of larval helpers, and varying numbers of sibling neotenic queens to assess the impact of secondary polygyny to the individual and colony. Under monogyne conditions, neotenics developed more ovarioles per ovary and had higher individual fecundities after 60 d compared with females under polygyne conditions. Queens in groups of three females were able to gain more body mass than those in groups of Þve. Although the division of resources provided by helpers reduced individual female development and fecundity under polygyne conditions, it resulted in an overall increase in colony fecundity. In addition, neotenic females in polygynous colonies did not differ signiÞcantly in reproductive competence. There was no evidence that neotenics were attacked or injured by other reproductives or larval helpers, suggesting little if any reproductive competition among sibling queens. The physiological responses of neotenics to the increasing queen/worker ratio may have the beneÞt of enhancing the colony growth at the cost of the fecundity of individual queens.

KEY WORDS reproductive skew, neotenic reproductives, inclusive Þtness, reproductive plasticity, inbreeding

In social insects, a division of labor between repro- existence of multiple queens is common, the fecundity ductive and worker castes enables a queen to direct of each queen may be reduced (Thorne 1982, 1984, nutritional resources toward oogenesis, facilitating 1985, Keller and Vargo 1993, Kaib et al. 2001). In this rapid colony growth (Oster and Wilson 1978, Porter case, a decline in the per capita rate of egg production and Tschinkel 1986, Tschinkel 1988, Keller and Vargo may occur through equal reductions in all queens, 1993). As colony size increases, a reproductive female lowering the variance in their fecundities. Alterna- will eventually become saturated with help, and the tively, a dominant queen might inhibit oogenesis in rate at which she lays eggs will be determined by her subordinates, thereby creating high variance in queen physiological limitations (Oster and Wilson 1978, fecundities, as occurs in some wasps (Gibo 1978, West- Tschinkel 1988). Secondary polygyny (Ho¨lldobler Eberhard 1969), ants (Ross 1988, Ho¨lldobler and Wil- and Wilson 1977), which regularly occurs in many son 1990), and possibly the termite Nasutitermes prin- species of the lower termites (reviewed in Miller 1969, ceps (Roisin and Pasteels 1985). Myles and Nutting 1988, Roisin 1993, Myles 1999), may Although several studies using natural populations allow colony growth to exceed the physiological lim- of termites have shown a negative correlation be- itation of individual queen fecundity (Darlington tween queen number and individual fecundity as mea- 1985, Roisin 1993). However, colony fecundity is still sured from oviposition rates (Roisin and Pasteels 1985, constrained by nutritive resources, particularly nitro- 1986, Kaib et al. 2001) or queen weight (an indicator gen, made available to queens (reviewed in LaFage of potential fecundity; Thorne 1982, 1984, 1985, Dar- and Nutting, 1978, Nalepa 1994). Some species bal- lington 1985, Lenz 1985, Roisin and Pasteels 1985, ance resource limitations and egg production by reg- 1986, Kaib et al. 2001), there have been no controlled ulating queen number, either through neglect or the experiments that directly measure the extent that ter- aggression of workers (Ruppli 1969, Mensa-Bonsu mite reproductives are affected by increasing resource 1976, Lenz 1985, Sieber 1985, Roisin and Pasteels 1986, partitioning. To examine the relationship of queen Miyata et al. 2004) or by intragroup competition be- number and individual queen fecundity, the repro- tween reproductives (Thorne 1985, Noirot 1990, Roi- ductive development of newly molted neotenic fe- sin 1993). For species in which the long-term co- males of Zootermopsis angusticollis Hagen was examined under monogynous and increasingly polygynous 1 Corresponding author: School of Life Sciences, Arizona State colony conditions. Dampwood termites are single- University, Tempe, AZ 85287-4501 (e-mail: [email protected]). piece nesters (Abe 1987), and long-lived polygynous 2 Department of Biology, Boston University, Boston, MA 02215. 3 Department of Entomology, North Carolina State University, Ra- associations of secondary (neotenic) reproductives leigh, NC 27695. are common in older colonies (Heath 1903, Castle

0046-225X/08/0883Ð0888$04.00/0 ᭧ 2008 Entomological Society of America 884 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 4

1934, Light and Illg 1945, unpublished data). The rate and Traniello 2001a, b). Neotenics were checked for of ovarian maturation and oocyte production of Z. evidence of agonistic interactions (bite marks and angusticollis neotenics has been shown to be inßu- missing or damaged legs and antennal segments) and enced by the availability of larval helpers that supply weighed to determine change in body mass. The per- the reproductives with nutrients (Greenberg and Stu- cent change in mass was used as an estimate of the art 1979; Brent and Traniello 2001b). Increasing the availability of endogenous resources above what is proportion of queens relative to helpers should there- used toward ovarian development and activity. Be- fore affect reproductive development. Here we ex- cause it is a relative measure, it is not inßuenced by amined how queen number inßuences individual and differences in initial mass caused by colony of origin. colony fecundity, assessing whether direct or indirect Termites were preserved individually in labeled 0.5-ml competition occurs among reproductive females as Eppendorf tubes containing 70% ethanol until dissec- colony resources become increasingly divided. tion. Both ovaries were removed, and the total number of functional ovarioles in each ovary was recorded. The number of vitellogenic oocytes and corpora lutea Materials and Methods was also noted to estimate of fecundity. Oocytes were Termites originated from stock colonies of Z. an- considered vitellogenic if their volume was Ն0.01 mm3 gusticollis collected in 1998 from the Redwood East (Brent and Traniello 2001a). In a number of colonies, Bay Regional Park, near Oakland, CA, and in 2004 from neotenic mortality led to the differentiation of new the Del Monte Forest in Pebble Beach, CA. Secondary neotenics from helper larvae. Monogynous colonies in reproductives (neotenics) were generated from which these changes occurred were not used, but data fourth- to seventh-instar larvae that were removed were collected from polygynous colonies that did not from Þve stock colonies and isolated in 14 groups of deviate from the original number of neotenic females 50Ð60 individuals that were all from the same colony. by more than one individual. These termites were placed in clear covered plastic Statistical analysis was performed using JMP v. 5.1 boxes (17 by 12 by 6 cm) containing moistened Þlter (SAS Institute 2002). Normally distributed data al- paper and small pieces of wood from their natal nest. lowed the use of analysis of variance (ANOVA) to ␣ ϭ The sex ratio of larvae is roughly equal for this species determine whether there were signiÞcant ( critical (unpublished data), and it was assumed the ratio was 0.05) differences between treatment groups on indi- maintained for each isolated group. Containers were vidual days. Probability values were adjusted for mul- visually surveyed on an approximately daily basis to tiple tests using Scheffe´ correction (Sokal and Rohlf detect neotenics, which were collected within 1Ð2 d of 1995). A two-tailed StudentÕs t-test was used to com- their adult molt. Three groups of experimental colo- pare the frequency of interactions of each female with nies were established, containing either 1 (n ϭ 24), 3 the male, larvae, and the other females. (n ϭ 23), or 5 female neotenics (n ϭ 14), in addition to 10 larvae (randomly mixed sexes, third or fourth Results instar) and 1 male neotenic. Before being placed in a colony, each female neotenic was weighed to deter- The Þrst neotenics began to differentiate within mine initial mass and given an identifying mark on the isolated groups of larvae 1 wk after isolation from the abdomen with enamel paint (TestorÕs). Ten larvae are inhibitory stimuli of reproductives, but the majority of adequate to ensure reproductive maturation in a mo- adult molts occurred after 4 wk. Across the isolated nogynous pair of secondary reproductives (Brent and groups of larvae, females developed into neotenics 2.7 Traniello 2001b), but there are sufÞciently few so that times more frequently than males, although groups adding neotenics produces a marked skew in such a varied (0.9Ð4.7), perhaps because of differences in queen/worker ratio. All colonies nested in covered the initial sex ratio in the isolated groups. plastic petri dishes (100 by 15 mm) containing Ϸ5g There were signiÞcant developmental differences (dry weight) of moistened birch wood. The dishes among neotenics maturing in monogynous and polyg- were placed in large covered plastic boxes with paper ynous colonies. Females maturing in polygynous col- towel liners moistened regularly to maintain humidity. onies of three queens had a signiÞcantly higher per- Colonies were maintained under a 14 L: 10 D light cent mass gain (Fig. 1; 44.77 Ϯ 1.90; n ϭ 57) than cycle at 23ЊC. A subset of 10 colonies was randomly females in monogynous colonies (35.04 Ϯ 2.54; n ϭ 24; selected from each treatment group for behavioral ANOVA, F ϭ 6.686, df ϭ 1, P ϭ 0.012) or polygynous analysis. During two 1-h long sessions for each of the colonies of Þve queens (38.25 Ϯ 1.83; n ϭ 61; ANOVA, Þrst 10 d after colony founding, all instances of ago- F ϭ 5.999, df ϭ 1, P ϭ 0.016). There was no signiÞcant nistic interaction (i.e., biting, lunging) between both difference in the mass gained by the reproductive reproductive and nonreproductive nestmates were re- females from the latter two groups (ANOVA, F ϭ corded. During the observation period, the termites 1.151, df ϭ 1, P ϭ 0.286). However, the number of were left under the same housing conditions as the ovarioles per ovary in females from monogynous col- unobserved termites to ensure similar development onies (32.04 Ϯ 0.83, n ϭ 24; Fig. 1) was signiÞcantly environments. greater than that observed in females developing in Termites were sampled 60 d after the colonies were polygynous colonies with three (27.95 Ϯ 0.51, n ϭ 57; initiated. This is an adequate time period for neotenics ANOVA, F ϭ 19.251, df ϭ 1, P Ͻ 0.0001) or Þve queens to mature reproductively and begin ovipositing (Brent (27.99 Ϯ 0.52, n ϭ 61; ANOVA, F ϭ 17.031, df ϭ 1, P Ͻ August 2008 BRENT ET AL.: BENEFITS AND COSTS OF SECONDARY POLYGYNY IN Z. angusticollis 885

48 b 34 Despite the physiological differences among fe- c 57 24 Mass Gain males maturing under different social conditions, Ovariole Number there seemed to be little developmental difference 44 32 between nestmate females maturing under the same a colony conditions. In colonies of three females, the 61 40 30 most fecund individuals did not signiÞcantly differ a d 24 d from the overall average for percent mass gain 57 61 (45.79 Ϯ 3.48 versus 44.77 Ϯ 1.90 ANOVA, F ϭ 0.061, 36 28 df ϭ 1, P ϭ 0.805), ovariole number (29.07 Ϯ 0.72 versus 27.95 Ϯ 0.51; ANOVA, F ϭ 1.740, df ϭ 1, P ϭ

Ovariole Number (mean + s.e.) 0.191), or fecundity (2.54 Ϯ 0.38 versus 1.70 Ϯ 0.36; Percent Mass Gain (mean + s.e.) 32 26 ANOVA, F ϭ 3.27, df ϭ 1, P ϭ 0.074). Similar results 1 3 5 were found in colonies with Þve neotenics; females Queen Number selected for having the highest fecundities did not Ϯ differ from the remaining neotenics in percent mass Fig. 1. Mean ( SE) percent mass gain (gray bars) and Ϯ Ϯ ϭ number of functional ovarioles per ovary (black bars) for gain (38.07 3.25 versus 38.25 1.56; ANOVA, F neotenic females in colonies with one, three, or Þve queens. 0.003, df ϭ 1, P ϭ 0.959) and ovariole number (29.25 Ϯ Sample sizes are provided. Bars having the same letter are not 1.01 versus 27.99 Ϯ 0.49; ANOVA, F ϭ 1.250, df ϭ 1, P ϭ signiÞcantly different (P Ͼ 0.05, one-way ANOVA with 0.267). Fecundity was signiÞcantly greater for the fe- Scheffe´ correction). males selected on this attribute (3.46 Ϯ 0.44 versus 1.69 Ϯ 0.33; ANOVA, F ϭ 13.016, df ϭ 1, P Ͻ 0.001), but when 100 replicates of the data set were run using 0.001). Similarly, individual fecundity was signiÞ- randomized assortment of the fecundity values, sim- cantly higher in females from monogynous colonies ilarly signiÞcant differences were found 16% of the (Fig. 2; 4.13 Ϯ 0.46, n ϭ 24) compared with that of time. This indicates there was no real difference females from polygynous colonies of three (1.70 Ϯ among neotenic fecundities within polygynous colo- 0.36, n ϭ 57; ANOVA, F ϭ 14.199, df ϭ 1, P Ͻ 0.001) nies beyond what might occur by chance. or Þve queens (1.69 Ϯ 0.33, n ϭ 61; ANOVA, F ϭ There was no physical or behavioral evidence of 16.150, df ϭ 1, P Ͻ 0.001). Females from the two aggression directed toward neotenics by other repro- polygynous groups did not differ signiÞcantly in either ductives or their larval helpers. Rather, neotenics ovariole number (ANOVA, F ϭ 0.004, df ϭ 1, P ϭ were occasionally observed allogrooming and spent 0.948) or fecundity (ANOVA, F ϭ 0.008, df ϭ 1, P ϭ most of their time in close proximity. Larvae appeared 0.960). Total colony fecundity varied among groups to provision and groom each reproductive to a similar (Fig. 2). Colonies with Þve female neotenics had the extent. Together with the developmental data, these highest cumulative fecundity (7.34 Ϯ 0.84, n ϭ 14), observations suggest that there is little if any direct or which was signiÞcantly greater than that observed in indirect competition between reproductives at this colonies with one (4.13 Ϯ 0.46, n ϭ 24; ANOVA, F ϭ stage in their maturation. 5.683, df ϭ 1, P ϭ 0.023) or three (4.22 Ϯ 0.89, n ϭ 23; ANOVA, F ϭ 4.627, df ϭ 1, P ϭ 0.039) female neotenics. There was no statistical difference in total fe- Discussion cundity for colonies with one or three queens The tendency for Z. angusticollis colonies with re- (ANOVA, F ϭ 0.006, df ϭ 1, P ϭ 0.940). placement reproductives to be polygynous seems to be the result of two factors. First, the rate of differ- 10 10 entiation of larvae into neotenics is skewed, favoring Individual c females over males. Similar data have previously been 14 8 Colony 8 reported for this species (Heath 1903, Castle 1934, Greenberg and Stuart 1982). Second, behavioral observations suggest that there is no immediate culling of 6 a 6 a a 22 supernumerary reproductives, by other reproductives 24 24 or larval helpers, as has been observed in other termite 4 4 species (reviewed in Roisin 1993, 2000, Myles 1999. It b b is possible that secondary culling occurs under natural 57 64 2 2 conditions or at some point later in the development of neotenics, but there is little supporting evidence. Colony Fecundity (mean + s.e.)

Individual Fecundity (mean + s.e.) Although other basal termites tend toward parity in 0 0 1 3 5 sex ratios of secondary reproductives, these species Queen Number normally have fewer reproductives in general (Myles Fig. 2. Mean (ϮSE) individual (gray bars) and collective 1999). Z. angusticollis seems to have a much higher colony (black bars) fecundities for neotenic females in col- tolerance for multiple neotenics, sometimes having onies with one, three, or Þve queens. Sample sizes are pro- dozens of neotenics in a single colony (Heath 1903, vided. Bars having the same letter are not signiÞcantly dif- Castle 1934, Greenberg and Stuart 1982, unpublished ferent (P Ͼ 0.05, one-way ANOVA with Scheffe´ correction). data). Although selection might favor a larger number 886 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 4 of coexisting females to increase colony growth, su- production of a greater number of highly related perßuous males should be selected against because nieces and nephews could compensate for a reduction only one or a few males are needed to provide ade- of direct Þtness caused by sharing nutritional re- quate sperm, the remainder adding only a metabolic sources (Darlington 1985, Crozier and Pamilo 1996). cost to the colony (Myles 1999). The added beneÞts would decrease the likelihood of Behavioral and developmental data for neotenic competition among the females. The high relatedness females maturing within the same colony indicate that of resulting offspring would also decrease selection in there is also little if any indirect competition between larvae to provision any given reproductive. However, secondaries to monopolize limited resources neces- the pattern we observed was for newly molted neo- sary for reproduction. There were no differences in tenics only, and individual reproductive capability the reproductive capabilities of neotenic nestmates, could become increasingly skewed among queens as which is likely the result of each female being cared reproductives and the colony mature. for by their larval helpers to the same extent. Termite For Z. angusticollis, in which the growth and max- reproductives, and neotenics in particular, are highly imum fecundity of a single primary female is physio- dependent on larvae, which can increase the energetic logically limited relative to the more advanced termite reserves of a female by transferring nutrients or by queens (Nutting 1969), secondary polygyny could be relieving the female of performing colony tasks an important adaptation to increase the rate at which (Rosengaus and Traniello 1993, Nalepa 1994, Brent colonies mature and exploit patchily distributed re- and Traniello 2001b). However, there seemed to be a sources (Darlington 1985, Roisin 1993). However, the cost to sharing resources. Because the number of lar- rate of colony growth could be constrained by the vae was held constant, increasing the number of neo- number of neotenics that develop and the number of tenic females resulted in fewer resources available to larvae available to support them. The results of our each reproductive. This resulted in monogynous fe- studies, which are the Þrst to control for the ages and males developing more ovarioles and having higher ratios of queens and workers and colony conditions, fecundities than individual polygynous females, and suggest that newly differentiated Z. angusticollis neo- females in groups of three acquiring more body mass tenics adjust their individual reproductive develop- than those in groups of Þve, despite similar resources ment and fecundity to match the colony conditions in expenditures on ovarioles and oocytes. which they develop. Reproductives limited by the It is possible that the reduced development of po- presence of few helpers or numerous neotenics com- lygynous females was not the result of partitioning pensate by producing fewer eggs. As the colony grows, colony nutritional resources, but may instead have the fecundity of each neotenic can be commensu- been caused by a subtle form of nestmate manipula- rately increased. Although we examined only the ear- tion. Polygynous reproductives of the ant Solenopsis liest stage of neotenic development, it is likely that this invicta use recognition cues to modulate each otherÕs responsiveness to colony conditions is retained development, causing an increasing degree of sup- throughout the life of the reproductives. It remains to pression with increasing queen number (Vargo 1992). be determined whether the adjustments in individual Pheromones probably trigger a neurohormonal cas- fecundity are the result of decreased care from larvae cade resulting in a decreased ovarian activity in S. or mutual inhibition between neotenics. invicta (Brent and Vargo 2003); a similar mechanism has been proposed for alates of this species (Brent et al. 2007). However, this seems an unlikely explanation Acknowledgments for Z. angusticollis neotenics given that pairing two We thank the administrators of the Redwood East Bay female neotenics does not have an effect on their Regional Park and the Pebble Beach Company for permission ovarian maturation and egg production that is discern- to collect termites and J. Brent, J. Dargin, and T. Juba for ibly different from pairing them with a male neotenic assisting with colony collection and maintenance. All exper- (Brent and Traniello 2001a). In this case, resource iments were conducted in accordance with U.S. statutes partition seems to be a more probable explanation governing research. The project was supported by the Na- than mutual inhibition. tional Research Initiative of the USDA Cooperative State The indirect Þtness gains from cooperative brood Research, Education and Extension Service Grant 2002- production may have reduced direct and indirect 35302-12526. competition among Z. angusticollis female neotenics. Although individual fecundity decreased as the num- References Cited ber of female neotenics increased, total colony fecundity increased. As neotenics mature and become more Abe, T. 1987. Evolution of life types in termites, pp. 139Ð152. fecund, such differences in reproductive potential In S. Kawano, J. H. Connell, and T. Hidaka (eds.), Evo- likely become more pronounced. Additionally, be- lution, coadaptation, and biotic communities. Kyoto Uni- cause of haplometrotic colony foundation (Heath versity Press, Kyoto, Japan. Brent, C. S., and J.F.A. Traniello. 2001a. Inßuence of sex- 1903, Castle 1934, Light 1934, Shellman-Reeve 1999, speciÞc stimuli on ovarian maturation in both primary Thorne et al. 2002), neotenics would normally be and secondary reproductives of the dampwood termite siblings and thus would mate with either a parent or Zootermopsis angusticollis. Physiol. Entomol. 26: 239Ð247. sibling, producing highly related offspring (Calleri et Brent, C. S., and J.F.A. Traniello. 2001b. Social inßuence of al. 2006). The increased inclusive Þtness gained in the larvae on ovarian maturation in primary and secondary August 2008 BRENT ET AL.: BENEFITS AND COSTS OF SECONDARY POLYGYNY IN Z. angusticollis 887

reproductives of the dampwood termite Zootermopsis Light, S. F., and P. Illg. 1945. Rate and extent of develop- angusticollis. Physiol. Entomol. 26: 78Ð85. ment of neotenic reproductives in groups of nymphs of Brent, C. S., and E. L. Vargo. 2003. Changes in juvenile the termite genus Zootermopsis (formerly Termopsis). hormone in maturing virgin queens of Solenopsis invicta. Univ. Cal. Publ. Zoo. 53: 1Ð40. J. Insect Physiol. 49: 967Ð974. Mensa-Bonsu, A. 1976. The production and elimination of Brent, C. S., C. Schal, and E. L. Vargo. 2007. Effects of social supplementary reproductives in Porotermes adamsoni stimuli on the endocrine systems of maturing queens of (Froggatt). Insectes Soc. 23: 133Ð154. the dampwood termite Zootermopsis angusticollis. Miller, E. M. 1969. Caste differentiation in the lower ter- Physiol. Entomol. 32: 26Ð33. mites, pp. 283Ð310. In K. Krishna and F. M. Weesner Calleri, D. V., E. M. Reid, R. B. Rosengaus, E. L. Vargo, and (eds.), Biology of termites, vol. 1. Academic, New York. J.F.A. Traniello. 2006. Inbreeding and disease resistance Miyata, H., H. Furuichi, and O. Kitade. 2004. Patterns of in a social insect: effects of heterozygosity on immuno- neotenic differentiation in a subterranean termite, Re- competence in the termite Zootermopsis angusticollis. ticulitermes speratus (Isoptera: Rhinotermitidae). Ento- Proc. Roy. Soc. Lond. B. 273: 2633Ð2640. mol. Sci. 7: 309Ð314. Castle, G. B. 1934. The damp-wood termites of western Myles, T. G. 1999. Review of secondary reproduction in ter- United States, genus Zootermopsis, pp. 264Ð282. In C. mites (Insecta: Isoptera) with comments on its role in ter- Kofoid (ed.), Termites and termite control. University of mite ecology and social evolution. Sociobiology 33: 1Ð91. California Press, Berkeley, CA. Myles, T. G., and W. L. Nutting. 1988. Termite eusocial Crozier, R. H., and P. Pamilo. 1996. Evolution of social in- evolution: a re-examination of BartzÕs hypothesis and sect colonies. Oxford University Press, New York. assumptions. Quart. Rev. Biol. 63: 1Ð23. Darlington, J.P.E.C. 1985. Multiple primary reproductives Nalepa, C. A. 1994. Nourishment and the origin of termite in the termite Macrotermes michaelseni (Sjo¨stedt), pp. eusociality, pp. 57Ð104. In J. H. Hunt and C. A. Nalepa 54Ð58. In J.A.L. Watson, B. M. Okot-Kotber, and Ch. (eds.), Nourishment and evolution in insect societies. Noirot (eds.), Caste differentiation in social insects. Per- Westview Press, San Francisco, CA. gamon, New York. Noirot, Ch. 1990. Sexual castes and reproductive strategies Gibo, D. L. 1978. The selective advantage of foundress as- in termites, pp. 5Ð35. In W. Engels (ed.), Social insects: an sociations in Polistes fuscatus (Hymenoptera: Vespidae): evolutionary approach to castes and reproduction. a Þeld study of the effects of predation on productivity. Springer, New York. Can. Entomol. 110: 519Ð540. Nutting, W. L. 1969. Flight and colony foundation, pp. 233Ð Greenberg, S.L.W., and A. M. Stuart. 1979. The inßuence of 282. In K. Krishna and F. M. Weesner (eds.), Biology of group size on ovarian development in adult and neotenic termites, vol. 2. Academic, New York. reproductives of the termite Zootermopsis angusticollis Oster, G. F., and E. O. Wilson. 1978. Caste and ecology in the Hagen (Hodotermitidae). Int. J. Invert. Reprod. 1: 99Ð social insects. Princeton University Press, Princeton, NJ. 108. Porter, S. D., and W. R. Tschinkel. 1986. Adaptive value of Greenberg, S.L.W., and A. M. Stuart. 1982. Precocious re- nanitic workers in newly founded red imported ant col- productive development (neoteny) by larvae of a prim- onies (Hymenoptera: Formicidae). Ann. Am. Entomol. itive termite Zootermopsis angusticollis (Hagen). Insectes Assoc. 79: 723Ð726. Soc. 29: 535Ð547. Heath, H. 1903. The habits of California termites. Biol. Bull. Roisin, Y. 1993. Selective pressures on pleometrosis and sec- 4: 47Ð63. ondary polygyny: a comparison of termites and ants, pp. 402Ð421. In L. Keller (ed.), Queen number and sociality Ho¨lldobler, B., and E. O. Wilson. 1977. The number of queens: an important trait in ant evolution. Naturwissen- in insects. Oxford University Press, New York. schaften 64: 8Ð15. Roisin, Y. 2000. Diversity and evolution of caste patterns, Ho¨lldobler, B., and E. O. Wilson. 1990. The ants. Belknap pp. 95Ð119. In T. Abe, D. E. Bignell, and M. Higashi (eds.), Press, Cambridge, United Kingdom. Termites: evolution, sociality, symbioses, ecology. Klu- Kaib, M., M. Hacker, and R. Brandl. 2001. Egg-laying in wer Academic Publishers, Boston, MA. monogynous and polygynous colonies of the termite Ma- Roisin, Y., and J. M. Pasteels. 1985. Imaginal polymorphism crotermes michaelseni (Isoptera, Macrotermitidae) In- and polygyny in the Neo-guinean termite Nasutitermes sectes Soc. 48: 231Ð237. princeps (Desneux). Insectes Soc. 32: 140Ð157. Keller, L., and E. L. Vargo. 1993. Reproductive structure Roisin, Y., and J. M. Pasteels. 1986. Replacement of repro- and reproductive roles in eusocial insect colonies, pp. ductive in Nasutitermes princeps (Desneux) (Isoptera: 16Ð44. In L. Keller (ed.), Queen number and sociality in Termitidae). Behav. Ecol. Sociobiol. 18: 437Ð442. insects. Oxford University Press, New York. Rosengaus, R. B., and J.F.A. Traniello. 1993. Temporal poly- LaFage, J. P., and W. L. Nutting. 1978. Nutrient dynamics in ethism in incipient colonies of the primitive termite Zoot- termites, pp. 165Ð232. In M. V. Brian (ed.), Production ermopsis angusticollis: a single multistage caste. J. Ins. ecology of ants and termites. Cambridge University Press, Behav. 6: 237Ð252. London, United Kingdom. Ross, K. G. 1988. Differential reproduction in multiple- Lenz, M. 1985. Is inter- and intraspeciÞc variability of lower queen colonies of the Þre ant Solenopsis invicta (Hy- termite neotenic numbers due to adaptive thresholds for menoptera: Formicidae). Behav. Ecol. Sociobiol. 23: neotenic elimination?Ñconsiderations from studies of 341Ð355. Porotermes adamsoni Froggatt (Isoptera: Termopsidae), Ruppli, E. 1969. Die Elimination u¨ berza¨hliger Ersatzge- pp. 125Ð146. In J.A.L. Watson, B. M. Okot-Kotber, and Ch. schlechtstiere bei der Termite Kalotermes ﬂavicollis Noirot (eds.), Caste differentiation in social insects. Per- (Fabr.). Insectes Soc. 16: 235Ð248. gamon, New York. SAS Institute. 2002. JMP statistics and graphics guide, ver- Light, S. F. 1934. The constitution and development of the sion 5.1 of JMP. SAS Institute, Cary, NC. termite colony, pp. 22Ð41. In C. Kofoid (ed.), Termites Shellman-Reeve, J. S. 1999. Courting strategies and conßicts and termite control. University of California Press, Berke- in a monogamous, biparental termite. Proc. Roy. Soc. ley, CA. Lond. B. Biol. Sci. 266: 137Ð144. 888 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 4

Sieber, R. 1985. Replacement of reproductives in Macrot- Thorne, B. L., N. L. Breisch, and M. I. Haverty. 2002. Lon- ermitinae (Isoptera, Termitidae), pp. 201Ð207. In J.A.L. gevity of kings and queens and Þrst time of production of Watson, B. M. Okot-Kotber, and C. Noirot (eds.), Caste fertile progeny in dampwood termite (Isoptera; Termop- differentiation in social insects. Pergamon, Oxford, sidae; Zootermopsis) colonies with different reproductive United Kingdom. structures. J. Anim. Ecol. 71: 1030Ð1041. Sokal, R. R., and F. J. Rohlf. 1995. Biometry, 3rd ed. W.H. Tschinkel, W. R. 1988. Social control of egg-laying rate in Freeman and Company, New York. queens of the Þre ant, Solenopsis invicta. Physiol. Ento- Thorne, B. L. 1982. Polygyny in termites: multiple primary mol. 13: 327Ð350. queens in colonies of Nasutitermes corniger (Motschul- Vargo, E. L. 1992. Mutual pheromonal inhibition among sky) (Isoptera: Termitidae). Insectes Soc. 29: 102Ð117. queens in polygyne colonies of the Þre ant Solenopsis Thorne, B. L. 1984. Polygyny in the Neotropical termite invicta. Behav. Ecol. Sociobiol. 31: 205Ð210. Nasutitermes corniger: life history consequences of queen West-Eberhard, M. J. 1969. The social biology of polistine mutualism. Behav. Ecol. Sociobiol. 14: 117Ð136. wasps. Misc. Publ. Mus. Zool., Univ. Mich. 140: 1Ð101. Thorne, B. L. 1985. Termite polygyny: the ecological dynamics of queen mutualism. Fortschritte Zool. 31: 325Ð341. Received 29 June 2007; accepted 2 January 2008.