William G. Eberhard

The tendency for the genital morphology of animals to diverge more rapidly than other traits is one of the most pervasive evolutionary patterns in animal form. Current controversy regarding explanations of this pattern stems in part from the difficulty of observing the behaviour of male genitalia during copulation. This limitation is reduced in tipuloid crane flies, because most of the male’s elaborate, divergent genital structures remain outside the female during copulation. Observations of genital behaviour during copulation in 45 species in 21 genera and subgenera, the most extensive sample of genital behaviour in any comparable group of animals, show a combination of trends that fits better with the stimulation version of the cryptic female choice hypothesis than with any of the other hypotheses commonly cited to explain rapid divergent genital evolution: sustained, rhythmic male genital movements such as brushing and tapping; frequent female facilitation of stimulation; lack of consistent morphological coevolution between corresponding male and female structures; lack of forceful male manipulations of females; lack of female “defenses” that impede male stimulation; and lack of direct male interference with other males’ sperm. Tipuloids are atypical among Diptera in generally lacking rhythmic, forceful genital thrusting and squeezing.

A new bridge between studies of sexual selection and the massive literature on C. elegans behavior and nervous system properties promises to provide important new insights in both fields. This paper shows that mate choice likely occurs in hermaphrodite C. elegans on the basis of stimulation from the male genital spicules, making it possible to apply the toolkit of extensive background knowledge of C. elegans and powerful modern techniques to test in unprecedented detail the leading hypotheses regarding one of the most sweeping trends in all of animal evolution, the especially rapid divergence of genital morphology. The recognition that sexual selection by mate choice may also occur in other contexts in C. elegans suggests additional payoffs from exploring previously unrecognized possibilities that female-active hermaphrodite reproductive behaviors are triggered by male stimulation. These facultative behaviors include attracting males, fleeing from or otherwise resisting males, opening the vulva to allow intromission, guiding sperm migration, avoiding rapid oviposition following copulation that results in sperm loss, expelling recently received sperm, and increasing feeding rates following copulation.

Male genitalia have been hypothesized to function as courtship devices during copulation, but it is difficult to use behavioral observations to test this hypothesis because male genitalia are usually hidden inside the female during copulation. In tipuloid flies, however, nearly all of the male’s complex genital structures remain outside the female. Copulation behavior and genital morphology in Tipula (Triplicitipula) colei and T. (Lunatipula) translucida suggest that some male genital structures function to stimulate the female: male structures that contact the female bear tufts or dense arrays of modified setae on precisely the surfaces that contact the female; contact involves repeated, stereotyped rhythmic movements that include brushing, vibrating, scraping, and tapping; the movements are appropriately designed to utilize the morphology of the modified setae to stimulate the female; and the movements have little or no other perceptible mechanical effects on the female. The female structures contacted by these male genital movements fail to show the defensive designs predicted by the theories of genital evolution that are based on morphological species isolation or male–female morphological conflicts of interest; also unexplained by the conflict of interest hypothesis are female movements that seem designed to increase rather than avoid stimulation by the male.

Orb-web construction behaviour, a classic example of ‘innate’ behaviour, is highly flexible. Determining which cues guide construction behaviour is complicated by the strong correlations between some variables, and the difficulty of manipulating of some web variables in biologically realistic ways. This study utilized a new experimental technique, adding sticky lines to webs during construction, to examine cues that guide sticky spiral spacing. Deflections and subsequent reductions in spacing produced by experiments that involved relatively long radii resembled the reduced spacing pattern on short radii in control webs; radius length was thus not the cue eliciting reduced spacing in control webs. An alternative, that smaller inter-radius distances elicited reduced spacing, was supported by experimentally removing radii to increase the distances between radii. The new technique also elicited variation in responses that suggested that spiders may use mental cues such as memories or expectations of line positions to guide sticky spiral placement.

Possible functions of several species-specific, sexually dimorphic male structures and of the male genitalia of Lytta eucera were deduced from observations of behaviour in the field and captivity, and were used to test theories of sexual selection. The male rubbed and tapped on the female’s antennae with sexually dimorphic segments of his antennae, and on her elytra with brushes of setae on his hind tarsi. He forcefully grasped the female’s prothorax and at least occasionally perforated the female’s prothoracic membranes with his modified middle tibiae, and her relatively uniform, membranous vaginal lining with his strong aedeagal teeth. His aedeagal teeth snagged her vaginal lining, and his gonostyli usually pressed against a featureless external female intersegmental membrane. None of these male structures was used as a weapon or in threat displays. No female structure fitted tightly in a “lock-and-key” manner with any of the male structures, nor was any female structure capable of selectively impeding their use, thus ruling out some hypotheses explaining their species-specificity in males. Female resistance to males, including occasional violent “tantrum” displays, was energetic, persistent, and highly effective; the functional significance of this resistance is unclear. If females distinguish the stimuli produced by species-specific traits of male genitalia, as supposed by some hypotheses, they likely use higher-level analyses in the central nervous system rather than the locations of the particular sense organs that are stimulated.

This first-ever extensive review of the construction behaviour of orb webs, of webs secondarily derived from orbs, and of non-orbs shows that the evidence favouring monophyly over convergent evolution of orbs is stronger than previously appreciated. The two major orb-weaving groups, Uloboridae and Araneoidea, share 31 construction behaviour traits, 20 of which are likely to be both derived and to have feasible alternatives, making convergence an unlikely explanation. Convergence in two lineages seems unlikely, and convergence in five different lineages, as proposed in some recent molecular studies of phylogeny, is even less credible. A further set of seven shared responses in orb design to experimentally constrained spaces also supports orb monophyly. Finally, a ‘control’ case of confirmed convergence on similar ‘pseudo-orbs’ in a taxonomically distant group also supports this argument, as it shows a low frequency of behavioural similarities. I argue that the omission of behavioural data from recent molecular studies of orb web evolution represents a failure of the analytic techniques, not the data, and increases the risk of making mistakes. In general, phylogenetic studies that aim to understand the evolution of particular phenotypes can benefit from including careful study of the phenotypes themselves.

Males of the agaonid wasp Heterandrium fallax have wing spots that they display during aggressive encounters near the ostioles of syconia of the fig Ficus pertusa, apparently in competition for the opportunity to copulate with emerging females. In accord with predictions of the “functional allometry hypothesis” for the allometry of structures that are under sexual selection as threat devices and that do not function as weapons, larger males tended to have proportionally larger wing spots. Some smaller males lacked spots, and smaller males were less likely to be collected near female emergence sites or to show antennal damage that probably results from male fights.

Studies of web evolution in spiders generally focus on the overall designs of webs in the field. As has been typical for dictynids and several other cribellate families with “irregular” webs, this study detected few discernable patterns in the field regarding the spatial organization of the highly variable, three-dimensional and largely aerial webs of the dictynid Dictyna meditata Gertsch, 1936. Nevertheless, there were three consistent sub-unit designs in the additions that spiders made to their webs in captivity, and in webs that they built from scratch in captivity: “silk ladders”, with a cribellum line that zig-zagged between a pair of approximately parallel non-sticky lines; “twig ladders”, with a cribellum line that zig-zagged between a non-sticky line and the substrate; and long non-sticky lines that each supported a long, slightly looped cribellum line. I suggest, using examples from dictynids and other families with long-lived, geometrically irregular webs, that this pattern of using consistent behavior patterns to add geometrically regular “modules”, is widespread and ancient, but has often been missed due to damage and additions to webs in the field, and to lack of direct behavioral observations. Recent attempts to link web evolution to studies of spider phylogeny could benefit from a change of emphasis, focusing on the additions that spiders make to their webs, rather than on the currently common but necessarily vague characterizations of overall web designs seen in the field.

In previous studies, the “cocoon” webs built by spiders of the genera Cyclosa Menge, 1866 and Allocyclosa Levi, 1999 under the influence of Polysphincta spp. wasps resembled molting webs built by unparasitized spiders; this behavioral manipulation was associated with increased concentrations of the molting hormone ecdysone. The present study documents an additional aspect of the cocoon webs of Allocyclosa bifurca (McCook, 1887) built under the influence of the wasp Polysphincta gutfreundi Gauld, 1991. Molting webs were more likely to have an associated barrier web than were prey capture orbs; and cocoon webs were even more likely to have barrier webs. The similarity between molting and cocoon webs accords with previous indications of ecdysone use by the wasps. The accentuation of molting web traits in the cocoon webs (also seen in other species) implies that the wasps manipulate the spiders using mechanisms other than simply replicating hormonal stimuli involved in normal molting.