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And Varroa Jacobsoni (Acari: Varroidae) Rev. Biol. Trop., 35(2): 209-214, 1987. Biological Analogies Between Sorne fig-wasps (Hymenoptera: Agaonidae and Torymidae: Sycophaginae) and Varroa jacobsoni (Acari: Varroidae) Williarn Ramírez B. Escuela de Fitotecnia, Facultad de Agronomía Universidad de Costa Rica (Received August 13, 1986) Abstract: Sorne fig wasps (Agaonidae and Torymidae: Sycophaginae) and the mi te Va"oa jacobsoni exhibit analogous biological, morphological and behavioral characteristics that seem to have arisen through conver­ gent evolution. Both groups develop in enclosed dark environments (small territories) with both high interna! humidity and carbon dioxide concentration. The males of both groups are haploid, exhibit neoteny, and ha ve shorter developmental phases and life spans than females. They do not fight at mating nor feed as adults. They are also less numerous and less sclerotized than the females. Male and female Varroa have enlarged peritremata and breathing tubes. Laminate breathing peritremal excrescenses or filaments are found in the Sycophaginae males (except Idarnes). The presence of large peritremata and protrudingbreathing structures, among other analogies between sorne fig wasps and the acarids, Varroa, seem to be adpatations to the humid environments in which they live during part of their life cycle. Organisms that develop in closed microenvironments (seraglia) with very similar and constant physical, biological and feeding conditions, seem to have very constant ontogenesis and also develop specific one-to-one relationships; that is, each host has a specific associate (parasite or symbiont). This type of association leads to radiative adaptations, synchronism of development for at least one of the associates and total dependence for at least one of the partners. They also show a high degree of relatedness. Both Agaonidae and Va"oa fit the "Local Mate Competition Rule" of Hamilton. Other characteristics that seem to fit into Hamilton's rule are: specific relationships between host and associate, developmental synchronization, associate females usually !ay a constant number of eggs; nearly constant developmental time from egg to adult of the associate, neotenic males, very constant ontogenies of one of the associates and precise sex ratios. The rnite Varroa jacobsoni Oud. (Varroidae) Another characteristic of very host-specific par­ is a parasite of the honey bees Apis cerana Fa­ asistes seern to be the neoteny of one of the sexes. bricius andA. mellifera L. (Apidae). In the lat­ Cornparative studies between organisrns that ter, it develops inside both the drone and work­ develop in similar environments or isolated er cells. The sycophilous wasps (Agonidae and food objects or hosts can produce clues to help Toryrnidae: Sycophaginae) develop exclusively understand the biology of similar but unrelated inside of the syconia of the flgs (Ficus). organisrns. Similar constant isolated environ­ Organisrns that occupy similar habitats or rni­ rnents can induce the evolution of analogous croenvironments and srnall territories or sera­ adaptations in unrelated arthropods . This will glios often exhibit analogous biological charac­ be shown later in a cornparison of certain char­ teristics that arise through convergent evolution. acteristics of V. jacobsoni, an econornically im­ They also tend to develop specific relationships portant rnite parasite of the honey bee A mel­ with host associates. Arnong the arthropods, lifera, and sorne sycophilous flg wasp groups sorne common exarnples of convergence are: (Aganoidae and Toryrnidae). Such cornparisons the presence of gills in aquatic organisrns, the are not only of acadernic interest, they can also loss of pigrnentation and eyes in cave dwellers, be of great value for a better understanding of and the loss of appendages (e.g.legs and wings) the biology of the organisrns involved. The and other adult characteristics arnong parasites. rnost outstanding analogies between the flg 209 210 REVISTA DE BIOLOGIA TROPICAL FIG. l. Ventral view of the right side of the female m!­ te (Varroa jacobsoni (Varroidae, Mesostigmata: Acari na) (IP.gs removed) showing the peritremal tube (Pt). Pt After Akratanakul 197 5, plate l. FIG. 2. Ventral view of the male fig wasp Apocrypta perplexa (Sycophaginae: Torymidae) . Showing the peritrenal tubes (Pt). After Coquerel, 1855, Fig. 2. wasps (Agaonidae and sorne Torymidae: Syco­ phagini) and Va"oa jacobsoni (Varroidae) are respiratory protruding structures (Figs. 1 and of the arthropods listed by Hamilton ( 1967), 2), reproductive and behavioral traits, and pre­ which develop in isolated hosts having sib­ cise sex ratios. mating combined with arrhenotoky and span­ andry are hymenopterous insects (including DISCUSSION Agaonidae) and a few species of mites (e.g. Laelaptidae, Pyemotidae and Tarsonemidae ). The developmental stages of both V. jacob­ Green et al. ( 1982) suggest that an evolutionary soni (and other Varroidae) and the sycophilic advantage of arrhenotoky is that it makes pre­ fig wasps occur in enclosed, confmed, dark hu­ cise sex ra ti os possible, wich provide a selective rnid habitats (seraglios) and isolated hosts: the advantage in highly inbred parasitic wasps. sealed brood cell of the honey bee and the inte­ Sorne insects that develop in humid or rior of the f¡g syconium, respectively. In all fig aquatic environments have evolved large peritre­ wasps (Agaonidae and Toryrnidae) and in V. mata and breathing tubes These include: most jacobsoni the males reproduce by arrhenotoky, Cyclorrhapha, especially the Tubulifera fly lar­ a mode of reproductio'n that readily permits the vae (Fam. Syrphidae) and the hemipterans Ne­ production of biased (Hamilton 1967, Joseph pidae and Belostomatidae. Breathing tubes are 1984), and precise sex ratios. also found in most Sycophaginae males and in According to Halmilton (1967), it seems both sexes of Va"oa jacobsoni. Hilton, (1961) that male haploid organisms have found them­ points out that insect eggs that are in wet en­ selves preadapted to live in isolated niches or vironments or become submerged have envol­ hosts of the sort characterized by his model. ved chorionic plastrons which are used for gas The evolution of male haploidy has actually exchange. In sorne species that are immersed in accompanied, in severa! independent lines, an water there are plastrons bearing elongated res­ evolutionary trend to occupy such niches. Most piratory homs (e.g. sorne Muscidae); egg shells RAMIREZ: Analogíes between fig-wasps and Va"oa mítes 211 with plastrons bearing homs have evolved (section Sycomorns), at the beginning of the independently (they are not homologous) in at male phase (when the maJe fig wasps are eclo­ least fifteen species. sing from the galls), the ambient is very wet and Adult males of Apocrypta, Eukoebelea, liquid accumulates within the syconium. Sycophaga and Sycophagella fig wasps (Torymi­ Unlike sorne Sycophaginae fig wasps, female dae: Sycophaginae. sensu Wiebes 1976), which Varroa ha ve a pair of peritremal breathing tubes spend part of their life cycle in very humid en­ (poorly developed in males) which are movable. vironments, have large peritremata and laminate strongly looped and extrude distally from the breathing excrescenses or long ftlaments on the stigrna in the region of coxa IV (Delfinado and spiracles (Fig. 2) which are used as snorkels Baker 1974) (Fig. 2). The adult fertilized fe · while they are submerged. The large peritrema­ male rnite enters the brood cells, where she bur­ ta and breathing tu bes of female Varroa (Fig. 1) ies herself in the larval food under the bee larva seem to be used for respiration while they are with its ventral side facing the larva. inactive and hidden in the wet brood food of Langhe and Natzkü (1977) postulated that the honey bee cell (De Jong 1984). When Va­ the peritremal tubes allow Varroa mites to rroa is submerged in the larval food of the bee, breath in the different gaseous regimes which the larva seems to be in a cataleptic state (Ra­ they encounter in the hives. While developing, mírez and Otis 1986). the mite must accommodate itself toa high car Sorne syconia of the Old World section bon dioxide concentration inside the hive or Sycocarpus contain a thick liquid or "liquor" at during flight of the bee. It is of interest to note a certain period of their development (Williams that Varroa has not been found in the nests of 1928, Baker 1913). This liquid can also be Apis dorsata and A. florea which build single found in the sections Sycomorns and exposed combs. Neomorphe ( sensu Ramírez 1977). In Ficus Flechtmann (197 5) mentions that the elon­ nota, this "liquor" is still present when the he­ gate peritremata on the stigma are found in teromorphous male wasps Agaonidae and the most predator rnites of suborder Mesostigmata, Sycophagini (farnily Torymidae) emerge from to which the Varroidae belong. The tubular the galls. Males of Eukoebelea nota have a pair peritremata are reduced or abstent in the endo­ of silvery tubes which extend intemally parasitic mites of vertebrates (Flechtmann throughout the length of the body and a pair of 1975). According to the same author much evi laminate excrescences or prong-like respiratory dence indicates that the tubular peritremata are processes which extend from the eighth uroter­ involved in the mechanisms of the hydrolic ba­ gite of the abdomen. These structures allow the lance of the mites (pers. com.). males to breath while they are submerged in the In heteromorphic fig wasps (Fam. Agaonidae "liquor" (Williams 1928). These respiratory ex­ and Torymidae: Sycophaginae) as well as Va­ tema! structures are a common syndrome in rroa (the bee mite) the males are smaller, neote­ most of the mate Sycophaginae, a parasitoid nic, and unpigmented . The similiraty of charac­ group of the Agaonidae (the pollinators). Wie­ teristics can be attributed to their development bes ( 1966, 197 6) informs that the gaster of in dark and humid microenviroments; namely, male Sycophaginae, except those of /darnes, the interior of the syconium and the brood cell bear very long, laminate excrescences on the respectively. The males of Agaonidae unlike the spiracles of the eighth urotergite.
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