Avoiding cuckoldry, lowered fitness, and untimely mortality while remaining a loving father: paternal egg brooding in the giant water bugs (HEMIPTERA: Belostomatidae).
John J. Lekovish
Of the more than one million described species of insects in the world, fewer than 150 exhibit the behavioral pattern of unilateral paternal care (Smith 1997). All of these species occur only in the order Hemiptera and nearly all of them occur only in the family Belostomatidae (Smith 1997). What is so extraordinary concerning the biology of the giant water bugs in order for this behavior to be selected? Several workers have intensively studied this question and have utilized the concepts of sexual selection and parental investment theory in composing the most plausible evolutionary scenario. Predation upon increasingly larger prey stemming from conspecific and intraspecific competition, the inordinate cost of egg production in comparison to egg brooding, and the development of strategies for paternity assurance appear to be the key ingredients in the formula (Smith 1997). Ultimately, it is hoped by workers that unraveling the obscure processes behind the evolution of exceptional behaviors will advance the overall understanding of evolution.
The elucidation of the evolutionary processes underlying exceptional behavioral patterns can be of considerable value to the understanding of the more widespread patterns exhibited in the class Insecta. Unilateral paternal care is certainly an exceptional behavior for insects. Fewer than 150 species, of the more than one million known to science, exhibit this behavior and nearly all of those are in the Hemipteran family Belostomatidae (Smith 1997). From what is understood of sexual selection and parental investment theory, this behavior is predicted to occur in species that have external fertilization, eggs or young that are particularly vulnerable to predation, face environmental extremes, and forage on patchy resources (Thornhill 1976; Ridley 1978; Borgia 1979; Zeh & Smith 1985). The above factors have little or no influence on the biology of an insect family having internal fertilization, relatively low mortality of progeny to predation, an aquatic habitat that buffers them against environmental extremes, and relatively abundant prey (Smith 1976, 1979; Venkatesan 1983; Ichikawa 1988; Smith & Larsen 1993).
A review of the literature pertaining to Belostomatids reveals that some genera have not been sufficiently studied (for instance, there exist no ecological descriptions for any species in Horvathinia). Furthermore, an enigmatic fossil record has made it a challenge for workers to discern a plausible scenario for the evolution of paternal care (Smith 1997). However, enough laboratory and field studies have been conducted on the egg brooding behavior of representative extant species to reveal valuable insights from which such a scenario has been constructed (Smith 1976, 1979; Venkatesan 1983; Ichikawa 1988, 1989; Kraus, 1989; Kraus, et al 1989; Smith & Larsen 1993). Dr. Robert L. Smith of the University of Arizona deserves much of the credit for the current understanding of the evolution of paternal care in the giant water bugs and a synopsis of this appears later in this paper.
The phylogeny and biology of Belostomatidae
The family Belostomatidae is divided into two subfamilies; Lethocerinae is comprised of a single genus while Belostomatinae is comprised of six genera (Smith 1997 after Lauck & Menke 1961; Mahner 1993). It is postulated that the Lethocerines are ancestral to the Belostomatines (Smith 1980; Smith & Larsen 1993; Smith 1997) With the exception of Limnogeton spp., all described Belostomatids possess natatorial middle and hind legs that are flat, broad, and fringed with hairs. These predators also possess, again with the exception of Limnogeton spp., raptorial forelegs with massive femora to firmly grasp prey. Smith (1997) comments that other workers consider the characters of Limnogeton as plesiomorphic from which the above were derived.
piercing/sucking mouthparts to inject potent proteolytic enzymes, within their saliva, into prey so as to imbibe the liquefying animal tissue. Most species are generalist foragers with the notable exceptions of species from two of the genera. All Limnogeton spp. are described as specialists on snails and it has been postulated that most Lethocerus spp. are at least facultative, if not obligate, vertebrate predators (Ichikawa 1988; Smith & Larsen 1993; Smith 1997).
The extraordinary feature distinguishing Belostomatids is, of course, the set of egg brooding behaviors performed exclusively by males. These brooding behaviors are divided into two types based on ovipositional substrate. Those behaviors exhibited in species in which females lay eggs on emergent vegetation of the aquatic habitat and those in species in which females lay eggs on the backs of males. Several behavioral studies indicate that brooding is obligatory for development and emergence of larvae from eggs (Smith 1976, 1979; Venkatesan 1983; Ichikawa 1988, 1995; Smith & Larsen 1993). Kraus, Gonzales, and Vehrencamp (1989) were able to demonstrate hatching from non-brooded egg pads and suggest that paternal care is adaptively advantageous but less siginificantly so than thought by other workers. Regardless, the pinnacle of brooding behaviors is probably the back-brooding exhibited by males of certain Belostomatine genera. This adaptation is the most novel and would seem to have been the most recently derived (Smith 1980, 1997; Zeh & Smith 1985).
Tallamy (1995) proposes an 'enhanced fecundity' hypothesis asserting that the costs of brooding to males are far less than those to females in producing eggs. The oppurtunity to continue to put maximal effort into foraging and thus provision more eggs may have selected for abandonment by females (Tallamy 1995). With the advent of the paternity assurance mechanism of repeatedly alternating copulation and oviposition, the major impediment to selection for brood care by males was removed (Smith 1980, 1997). Despite the aforementioned contradiction, field studies indicate that related costs to males such as impaired swimming and foraging abilities, apparency to potential predators, and energy expended to clean and aerate eggs are signficantly outweighed by the increase in the males fitness through increased progeny survivorship (Kraus, et al 1989; Smith & Larsen 1993).
The "Smith Hypothesis" of the evolution of paternal care in Belostomatidae
Smith (1997) surmises from the available data from cladistic analyses of the superfamily Nepoidea that the large size of it's members is a derived character and that the ancestor was a relatively small insect from the Upper Jurassic. From the fossil record it can be inferred that the primary habitats of this ancestor were shallow, temporary waters where it competed with Odonate larvae (Smith 1997). Those larger individuals capable of feeding on fish and amphibian larvae not available to smaller conspecifics would have enjoyed a considerable competitive advantage (Smith 1997). Smith (1997) agrees with the large body of evidence suggesting that five instars is plesiomorphic and unalterable for most Heteropteran species and thus the resulting race to become "bigger" could only have been won by selection for larger eggs. How then does an aquatic insect overcome the resultant decrease in gas exchange capacity from the decrease in the ratio of surface area to volume? Smith (1997) assumes this to be the catalyst that selected for oviposition on emergent vegetation where atmospheric oxygen would diffuse into eggs much more readily (~324,000 times more readily). In teleological terms, the unforeseen constraint would have been dessication of eggs lacking the complex chorionic structure of terrestrial insects. Smith (1997) postulates that a concomitant selection for parental care, provided by the male for reasons previously discussed, during selection for emergent oviposition would have been necessary for progeny survivorship. What then prompted the evolution of back-brooding among certain Belostomatine genera? Here the picture is more obscured but again Smith (1997) presents the most plausible scenario. Some gravid females may have accidentally oviposited on mate-guarding males or perhaps as a result of the lack of ovipositional substrates in the habitat. This development permits dispersal to and exploitation of habitats that were previously unsuitable.
Numerous examples exist in nature of quite extraordinary adaptations resulting from quite ordinary selection pressures. This may be the case with Belostomatidae and the evolution of their very unique reproductive system. This family includes some of the largest and most voracious predatory insects in the world. Again, if teleological terms may be permitted, this is the system that seems to function best for an insect that occupies this ecological niche.
Borgia, G. 1979. Sexual selection and the evolution of mating systems. In Sexual Selection and Reproductive Competition in Insects. M. S. Blum and N. A. Blum, eds., pp. 19-73. New York: Academic Press.
Ichikawa, N. 1988. Male brooding behaviour of the giant water bug Lethocerus deyrollei Vuillefroy (Hemiptera: Belostomatidae). J. Ethol. 6: 121-127.
Ichikawa, N. 1989. Breeding strategy of the male brooding water bug Diplonychus major Esaki (Hemiptera: Belostomatidae): Is male back space limiting? J. Ethol. 7: 133-140.
Ichikawa, N. 1995. Male counterstrategy against infanticide of the female giant water bug Lethocerus deyrollei (Hemiptera: Belostomatidae). J. Insect Behav. 8: 181-188.
Kraus, W. F. 1989. Is male back space limiting? An investigation into the reproductive demography of the giant water bug, Abedus indentatus (Heteroptera: Belostomatidae). J. Insect Behav. 2: 623-648.
Kraus, W. F., M. J. Gonzales, and S. L. Vehrencamp. 1989. Egg development and an evaluation of some of the costs and benefits for paternal care in the Belostomatid, Abedus indentatus (Heteroptera: Belostomatidae). J. Kansas Entomol. Soc. 62: 548-562.
Ridley, M. 1978. Paternal care. Anim. Behav. 26: 904-932.
Smith, R. L. 1976. Brooding behavior of a male water bug, Belostoma flumineum (Hemiptera: Belostomatidae). J. Kansas Entomol. Soc. 49: 333-343.
Smith, R. L. 1979. Paternity assurance and altered roles in the mating behaviour of a giant water bug, Abedus herberti (Heteroptera: Belostomatidae). Anim. Behav. 27: 716-725.
Smith, R. L. 1980. Evolution of exclusive postcopulatory paternal care in the insects. Fla. Entomol. 63: 65-78.
Smith, R. L. 1997. Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). In Social Behavior in Insects and Arachnids. J. C. Choe and B. J. Crespi, eds., 116-149. London: Cambridge University Press.
Smith, R. L. and E. Larsen. 1993. Egg attendance and brooding by males of the giant water bug Lethocerus medius (Guerin) in the field (Heteroptera: Belostomatidae). J. Insect Behav. 6: 93-106.
Tallamy, D. W. 1995. Nourishment and the evolution of paternal investment in subsocial arthropods. In Nourishment and Evolution in Insect Societies. J. H. Hunt and
C. A. Nalepa, eds., pp. 21-55. Boulder, CO Westview Press. Thornhill, R. 1976. Sexual selection and paternal investment in insects. Am. Nat. 110: 153-163.
Venkatesan, P. 1983. Male brooding behaviour of Diplonychus indicus Venk. And Rao (Hemiptera: Belostomatidae). J. Kansas Entomol. Soc. 56: 80-87.
Zeh, D. W. and R. L. Smith. 1985. Paternal investment by terrestrial arthropods. Am. Zool. 25: 785-805.