Complex behavioral plasticity is not reduced in spiderlings with miniature brains.

The brains of smaller animals are smaller than those of their larger relatives, but it is not clear whether their adaptive behavioral flexibility is more limited. Previous interspecific comparisons found that aspects of web construction behavior of very small orb weaving spiders (0.005 mg) were no less precise than those of much larger related orb weavers (30 mg), but the behaviors tested were relatively simple. Here we perform a more sensitive intraspecific test involving the multiple behavioral adjustments of orb web designs made by Leucauge argyra to confinement in very small spaces. Web adjustments of spiderlings as small as ~0.1 mg were compared to previously published observations of ~80 mg conspecific adults. Spiderlings in constrained spaces made all of the complex adjustments made by adults in at least seven independent web design variables, and their adjustments were no less precise. Rough estimates based on previously published data on total brain volumes and the mean diameters of neuron cell bodies suggested that spiderlings and adult females of Leucauge may have similar numbers of neurons, due to spiderlings having smaller neurons and a greater percentage of body tissues dedicated to the brain. We speculate that this neural similarity may explain why L. argyra spiderlings showed no behavioral deficits compared with adults.

Demonstrating sexual selection by cryptic female choice on male genitalia: What is enough?

Rapid divergence in external genital structures occurs in nearly all animal groups that practice internal insemination; explaining this pattern is a major challenge in evolutionary biology. The hypothesis that species-specific differences in male genitalia evolved under sexual selection as courtship devices to influence cryptic female choice (CFC) has been slow to be accepted. Doubts may stem from its radical departure from previous ideas, observational difficulties because crucial events occur hidden within the female's body, and alternative hypotheses involving biologically important phenomena such as speciation, sperm competition, and male-female conflicts of interest. We assess the current status of the CFC hypothesis by reviewing data from two groups in which crucial predictions have been especially well-tested, Glossina tsetse flies and Roeseliana (formerly Metrioptera) roeselii bushcrickets. Eighteen CFC predictions have been confirmed in Glossina and 19 in Roeseliana. We found data justifying rejection of alternative hypotheses, but none that contradicted CFC predictions. The number and extent of tests confirming predictions of the CFC hypothesis in these species is greater than that for other generally accepted hypotheses regarding the functions of nongenital structures. By this criterion, it is reasonable to conclude that some genital structures in both groups likely involved sexual selection by CFC.

Why the Static Allometry of Sexually-Selected Traits Is So Variable: The Importance of Function.

Sexually-selected traits often show positive static allometry, with large individuals bearing disproportionately large structures. But many other sexually-selected traits show isometry or even negative allometry, with trait size varying relatively little with body size. We recently proposed that the functions of these traits (as aggressive signals, weapons, courtship signals, and contact courtship devices) determine their allometries. Positive allometry is generally favored for aggressive signals because aggressive signals are selected to emphasize body size (and thus fighting prowess). In contrast, the biomechanics of force application in weapons only sometimes select for positive allometry; the content of courtship signals is even less often related to body size; and contact courtship devices are selected to be relatively invariant across body sizes. Here we summarize the arguments in favor of this "functional allometry" hypothesis and expand a comparative test of its predictions. Our results indicate that sexual traits have the allometric slopes predicted by our hypothesis, regardless of which body part bears the structure.

The allometry of CNS size and consequences of miniaturization in orb-weaving and cleptoparasitic spiders.

Allometric studies of the gross neuroanatomy of adults from nine species of spiders from six web-weaving families (Orbicularia), and nymphs from six of these species, show that very small spiders resemble other small animals in having disproportionately larger central nervous systems (CNSs) relative to body mass when compared with large-bodied forms. Small spiderlings and minute adult spiders have similar relative CNS volumes. The relatively large CNS of a very small spider occupies up to 78% of the cephalothorax volume. The CNSs of very small spiders extend into their coxae, occupying as much as 26% of the profile area of the coxae of an Anapisona simoni spiderling (body mass < 0.005 mg). Such modifications occur both in species with minute adults, and in tiny spiderlings of species with large-bodied adults. In at least one such species, Leucauge mariana, the CNS of the spiderling extends into a prominent ventral bulge of the sternum. Tiny spiders also have reduced neuronal cell body diameters. The adults of nearly all orbicularian spiders weave prey capture webs, as do the spiderlings, beginning with second instar nymphs. Comparable allometric relations occur in adults of both orb-weaving and cleptoparasitic species, indicating that this behavioral difference is not reflected in differences in gross CNS allometry.

Experiments with genitalia: a commentary.

There has been a recent burst of studies of the function of genitalia, many of which share several important shortcomings. Given that further studies on this topic are likely (there are probably millions of species showing rapid genital divergence), I discuss the studies critically to promote clear formulation of hypotheses and interpretation of results in the future. I also emphasize some possibly important but neglected variables, including female stimulation, phylogenetic contexts, and the behavior of male genitalia, and outline simple techniques that could improve future studies.

Evolution of genitalia: theories, evidence, and new directions.

Many hypotheses have been proposed to explain why male intromittent genitalia consistently tend to diverge more rapidly than other body traits of the same individuals in a wide range of animal taxa. Currently the two most popular involve sexual selection: sexually antagonistic coevolution (SAC) and cryptic female choice (CFC). A review of the most extensive attempts to discriminate between these two hypotheses indicates that SAC is not likely to have played a major role in explaining this pattern of genital evolution. Promising lines for future, more direct tests of CFC include experimental modification of male genital form and female sensory abilities, analysis of possible male-female dialogues during copulation, and direct observations of genital behavior.

Genitalic stridulation during copulation in a species of crane fly, Tipula (Bellardina) sp. (Diptera: Tipulidae) / Estridulación genital durante la cópula en una especie de mosca grulla, Tipula (Bellardina) sp. (Dípteros: Tipulidae)

The male genitalia of many animal groups have elaborate and species-specific forms. One hypothesis  to explain why this is so is that male genitalia function as stimulatory devices that are under sexual selection by cryptic female choice. This report is based on a videotaped observation of a single male of an unidentified species of Tipula (Bellarina) from San José Province, Costa Rica. A male crane fly stridulated (produced vibrations) during copulation using sustained and stereotyped movements of file and scraper structures on his genitalia. Males of related species have similar file and scraper structures on their genitalia, suggesting that they probably also stridulate during copulation. Rev. Biol. Trop. 57 (Suppl. 1): 251-256. Epub 2009 November 30.

Un macho de Tipula (Bellardina) sp. estriduló (produjo vibraciones) por medio de movimientos estereotipados de estructuras de sus órganos genitales durante varios minutos de la cópula. Los machos de algunas especies relacionadas poseen estructuras similares, lo cual sugiere que también estridulan durante la cópula.

Postcopulatory sexual selection: Darwin's omission and its consequences.

In one of his few major oversights, Darwin failed to appreciate that male-male competition and sexual selection can continue even after copulation has begun. The postcopulatory equivalents of both direct male-male battles (sperm competition) and female choice (cryptic female choice) occur within the female's body. Recognition of this hidden, but intense, sexual competition provides new insights into a variety of fields. These include the hyperdiverse and paradoxically elaborate morphology of both sperm and male genitalia, the equally puzzling and elaborate morphology of nongenitalic male structures that are specialized to grasp and stimulate females, powerful manipulative effects of substances in male semen on female reproductive physiology, paradoxical male courtship behavior that occurs after copulation has already begun, variability in parental investments, and the puzzlingly complex and diverse interactions between sperm and female products that surround animal eggs and between male gametophytes and female tissues in flowering plants. Many bizarre traits are involved, including male genitalia that are designed to explode or fall apart during copulation leaving behind parts within the female, male genitalia that "sing" during copulation, potent seminal products that invade the female's body cavity and her nervous system to influence her behavior, and a virtual Kama Sutra of courtship behavior performed after rather than before genital coupling, including male-female dialogues during copulation.

Experimental modifications imply a stimulatory function for male tsetse fly genitalia, supporting cryptic female choice theory.

One of the most sweeping of all patterns in morphological evolution is that animal genitalia tend to diverge more rapidly than do other structures. Abundant indirect evidence supports the cryptic female choice (CFC) explanation of this pattern, which supposes that male genitalia often function to court females during copulation; but direct experimental demonstrations of a stimulatory function have been lacking. In this study, we altered the form of two male genital structures that squeeze the female's abdomen rhythmically in Glossina pallidipes flies. As predicted by theory, this induced CFC against the male: ovulation and sperm storage decreased, while female remating increased. Further experiments showed that these effects were due to changes in tactile stimuli received by the female from the male's altered genitalia, and were not due to other possible changes in the males due to alteration of their genital form. Stimulation from male genital structures also induces females to permit copulation to occur. Together with previous studies of tsetse reproductive physiology, these data constitute the most complete experimental confirmation that sexual selection (probably by CFC) acts on the stimulatory properties of male genitalia.

Static allometry and animal genitalia.

A survey of 117 species of arthropods and 17 species of vertebrates showed a strong trend for male genitalia to have relatively low static allometric values. This trend contrasts with the allometry of other structures under sexual selection, which usually show steep allometric slopes. The trend to low allometric genital values is less consistent in mammals than in arthropods. Data not in accord with the previous the "one-size-fits-all" explanation for low allometric slopes in genitalia, which was based on sexual selection by female choice, suggest a more general version that includes both natural selection and sexual selection, and involves both mechanical fit and stimulation. Less-complete data on the female genitalia of arthropods suggest a trend to similar low allometric slopes, and may also be explained by mechanical fit and stimulatory one-size-fits-all arguments.

Seasonal patterns of parasitism of the tropical spiders Theridion evexum (Araneae, Theridiidae) and Allocyclosa bifurca (Araneae, Araneidae) by the wasps Zatypota petronae and Polysphincta gutfreundi (Hymenoptera, Ichneumonidae)

The rates of parasitism of Theridion evexum by the parasitoid wasp Zatypota petronae, and Allocyclosa bifurca by Polysphincta gutfreundi, were followed for two years. Parasitism of T. evexum was very low (mean 1.39+1.8%), and restricted to nearly seven months of the year. Parasitism of A. bifurca was higher (mean 7.8+7.6%), and did not show a seasonal pattern. Reproduction of the host spider T. evexum was highly seasonal, with only one, highly coordinated generation per year, while adults of A. bifurca were present year round. Short-term autocorrelation on parasitism rates over time at different sites suggest that P. gutfreundi tend to return to the same sites to hunt hosts over periods of a few weeks. Rev. Biol. Trop. 56 (2): 749-754. Epub 2008 June 30.

Las tasas de parasitismo de Theridion evexum por la avispa parasitoide Zatypota petronae y de Allocyclosa bifurca por Polysphincta gutfreundi fueron estudiadas durante dos años. El parasitismo en T. evexum fue muy bajo (promedio 1.39+1.8%) y restringido a aproximadamente siete meses del año. El parasitismo en A. bifurca fue más alto (promedio 7.8+7.6%) y no mostró un claro patrón estacional. La reproducción de la araña hospedera T. evexum fue muy estacional, con solamente una generación por año, mientras que los adultos de A. bifurca estuvieron presentes todo el año. Autocorrelaciones de las tasas de parasitismo entre censos consecutivos en diferentes sitios sugiere que P. gutfreundi tiende a retornar a los mismos sitios para parasitar las arañas hospederas durante algunas semanas.

Seasonal patterns of parasitism of the tropical spiders Theridion evexum (Araneae, Theridiidae) and Allocyclosa bifurca (Araneae, Araneidae) by the wasps Zatypota petronae and Polysphincta gutfreundi (Hymenoptera, Ichneumonidae).

The rates of parasitism of Theridion evexum by the parasitoid wasp Zatypota petronae, and Allocyclosa bifurca by Polysphincta gutfreundi, were followed for two years. Parasitism of T. evexum was very low (mean 1.39 +/- 1.8%), and restricted to nearly seven months of the year. Parasitism of A. bifurca was higher (mean 7.8 +/- 7.6%), and did not show a seasonal pattern. Reproduction of the host spider T evexum was highly seasonal, with only one, highly coordinated generation per year, while adults of A. bifurca were present year round. Short-term autocorrelation on parasitism rates over time at different sites suggest that P. gutfreundi tend to return to the same sites to hunt hosts over periods of a few weeks.

Miniaturized orb-weaving spiders: behavioural precision is not limited by small size.

The special problems confronted by very small animals in nervous system design that may impose limitations on their behaviour and evolution are reviewed. Previous attempts to test for such behavioural limitations have suffered from lack of detail in behavioural observations of tiny species and unsatisfactory measurements of their behavioural capacities. This study presents partial solutions to both problems. The orb-web construction behaviour of spiders provided data on the comparative behavioural capabilities of tiny animals in heretofore unparalleled detail; species ranged about five orders of magnitude in weight, from approximately 50-100mg down to some of the smallest spiders known (less than 0.005mg), whose small size is a derived trait. Previous attempts to quantify the 'complexity' of behaviour were abandoned in favour of using comparisons of behavioural imprecision in performing the same task. The prediction of the size limitation hypothesis that very small spiders would have a reduced ability to repeat one particular behaviour pattern precisely was not confirmed. The anatomical and physiological mechanisms by which these tiny animals achieve this precision and the possibility that they are more limited in the performance of higher-order behaviour patterns await further investigation.

Fitting together: copulatory linking in some Neotropical Chrysomeloidea

Copulatory linking of male and female genitalic structures in 11 Neotropical species of Chrysomelidae and one species of Megalopodidae was studied by freezing and then dissecting pairs of beetles in copula. In Megalopus armatus (Megalopodidae) the male has a long endophallus with complex membranous protuberances and a terminal flagellum that probably reaches the spermatheca. In the subfamily Eumolpinae the females have telescoping ovipositors through which the male endophalli pass, reaching to or near the mouth of the spermathecal duct. A long thin flagellum is probably inserted into the spermathecal duct. The male endophalli are braced inside the female using various structures, including two pairs of lateral appendages and apical appendages (both lateral pairs sclerotized in Colaspis sanjoseana and only the basal pair in Brachypnoea irazuensis), a pair of membranous swellings (in Metaxyonycha amasia), and apical microspicules on the endophallus (in Xanthonia). In the subfamily Galerucinae, males of Metrioidea and Diabrotica (tribe Galerucini) have relatively short endophalli ornamented with sclerotized hooks, spines and needles. In Metrioidea elongata the long needle-like endophallic spines of the male were erected inside the female and penetrated the wall of her bursa. In the tribe Alticini, the male endophallus is very short and does not enter the female in two species, Alagoasa gemmata and Walterianella sp. Instead, the apical parts of the female bursae were everted, and were clamped by sclerites of the male median lobe. The male genitalia of Plectrotetra hirsuta reached deep into the female, to the median oviduct, far beyond the mouth of the spermathecal duct. Both rigid and membranous structures meshed in complex ways. When these observations are combined with published descriptions of mating in other Chrysomelidae, the great diversity of copulatory morphology in these families comes into sharper focus.

Se describen los coajustes mecánicos entre las estructuras genitales de machos y hembras de 11 especies neotropicales de Chrysomelidae y una especie de Megalopodidae. Las parejas fueron congeladas durante la cópula y después disectadas. En Megalopus armatus (Megalopodidae) el macho tiene un endofalo largo, con protuberancias membranosas complejas, y un flagelo terminal que probablemente penetra el largo del ducto de la espermateca hasta el lumen de la espermateca. En la subfamilia Eumolpinae, las hembras tienen ovipositores telescópicos, a través de los cuales los endofali de los machos pasan para llegar hasta o cerca a la boca del ducto de la espermateca. Es probable que el largo y delgado flagelo se inserta en el ducto de la espermateca. El endofalo del macho se apoya dentro de la hembra por varias estructuras, las cuales incluyen dos pares de apéndices laterales y apéndices apicales (ambos pares laterales son esclerotizados en Colaspis sanjoseana, únicamente el par basal en Brachypnoea irazuensis), un par de hinchamientos membranosos (en Metaxyonycha amasia), y espículas apicales sobre el endofalo (en Xanthonia). En la subfamilia Galerucinae, los machos de Metrioidea y Diabrotica (tribu Galerucini) tienen endofalos relativamente cortos, pero adornados con varios ganchos, espinas y agujas. En Metrioidea elongata las largas espinas endofálicas se abrieron dentro de la hembra, y penetraron las paredes de su bursa. En la tribu Alticini, el endofalo del macho de dos especies, Alagoasa gemmata y Walterianella sp., es muy corto y no entró al cuerpo de la hembra. En su lugar, la parte apical de la bursa de la hembra fue evertida, y fue agarrada por escleritos del lóbulo mediano del macho. Los genitales de Plectrotetra hirsuta penetraron profundamente en la hembra, llegando probablemente hasta el oviducto mediano, más profundo que la boca del ducto de la espermateca. Estructuras de...

Tie them up tight: wrapping by Philoponella vicina spiders breaks, compresses and sometimes kills their prey.

We show that uloborid spiders, which lack the poison glands typical of nearly all other spiders, employ thousands of wrapping movements with their hind legs and up to hundreds of meters of silk line to make a shroud that applies substantial compressive force to their prey. Shrouds sometimes break the prey's legs, buckle its compound eyes inward, or kill it outright. The compressive force apparently results from the summation of small tensions on sticky lines as they are applied to the prey package. Behavioral details indicate that wrapping is designed to compact prey; in turn, compaction probably functions to facilitate these spiders' unusual method of feeding. This is the first demonstration that prey wrapping by spiders compacts and physically damages their prey, rather than simply restraining them.

Fitting together: copulatory linking in some Neotropical Chrysomeloidea.

Copulatory linking of male and female genitalic structures in 11 Neotropical species of Chrysomelidae and one species of Megalopodidae was studied by freezing and then dissecting pairs of beetles in copula. In Megalopus armatus (Megalopodidae) the male has a long endophallus with complex membranous protuberances and a terminal flagellum that probably reaches the spermatheca. In the subfamily Eumolpinae the females have telescoping ovipositors through which the male endophalli pass, reaching to or near the mouth of the spermathecal duct. A long thin flagellum is probably inserted into the spermathecal duct. The male endophalli are braced inside the female using various structures, including two pairs of lateral appendages and apical appendages (both lateral pairs sclerotized in Colaspis sanjoseana and only the basal pair in Brachypnoea irazuensis), a pair of membranous swellings (in Metaxyonycha amasia), and apical microspicules on the endophallus (in Xanthonia). In the subfamily Galerucinae, males of Metrioidea and Diabrotica (tribe Galerucini) have relatively short endophalli ornamented with sclerotized hooks, spines and needles. In Metrioidea elongata the long needle-like endophallic spines of the male were erected inside the female and penetrated the wall of her bursa. In the tribe Alticini, the male endophallus is very short and does not enter the female in two species, Alagoasa gemmata and Walterianella sp. Instead, the apical parts of the female bursae were everted, and were clamped by sclerites of the male median lobe. The male genitalia of Plectrotetra hirsuta reached deep into the female, to the median oviduct, far beyond the mouth of the spermathecal duct. Both rigid and membranous structures meshed in complex ways. When these observations are combined with published descriptions of mating in other Chrysomelidae, the great diversity of copulatory morphology in these families comes into sharper focus.

Evolutionary conflicts of interest: are female sexual decisions different?

Analyses of reproductive conflicts of interests have yielded important evolutionary insights in many areas of biology. The usefulness of conflict analyses of traits that have been traditionally interpreted as resulting from female choice is controversial, however. This article explores a possible explanation for why conflicts of interest may be ameliorated in female choice situations. In contrast to most other evolutionary contexts in which conflicts of interest are thought to have been important, sexual reproduction usually involves an extensive, irretrievable mixing of the genomes of the participants. Under certain combinations of costs and benefits to females, the genes in the female's genome can benefit, through increased reproduction of her offspring, from the very genes that produce sexually antagonistic traits in the male. In short, females can sometimes gain by "losing." Such Fisherian payoffs are also possible, though probably less important, for males. Gaining by losing is not feasible in most other contexts of evolutionary conflict, except under some conditions in parent-offspring conflict. Some apparent parent-offspring conflicts may instead be parental choice among offspring that is analogous to traditional female choice. Parent-offspring conflict may be relatively common, however, because offspring manipulation of their parents is likely to be damaging to the parents.

Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice.

Male structures specialized to contact females during sexual interactions often diverge relatively rapidly over evolutionary time. Previous explanations for this pattern invoked sexual selection by female choice, but new ideas emphasize possible sexually antagonistic coevolution resulting from male-female conflict over control of fertilization. The two types of selection have often not been carefully distinguished. They do not theoretically exclude one another, but they have not necessarily had equally important roles in producing rapid evolutionary divergence. To date, most recent empirical studies of antagonistic coevolution have emphasized only a few taxa. This study uses the abundant but little-used data in the taxonomic literature on morphology to evaluate the roles of antagonistic coevolution and traditional female choice over a wide taxonomic spectrum (61 families of arthropods, mostly insects and spiders). Groups with species-specific male structures that contact females were checked for coevolution of species-specific female structures that are contacted by the male and that have mechanical properties that could potentially defend her against the male. Facultatively deployable, species-specific female defensive structures, a design that would seem likely to evolve frequently under the sexually antagonistic coevolution hypothesis, were completely absent (0% of 106 structures in 84 taxonomic groups). Although likely cases of sexually antagonistic coevolution exist, using conservative criteria, 79.2% of the 106 structures lacked even potentially defensive female coevolution. A common pattern (53.8% of 106) was a nearly complete absence of female change in areas contacted by species-specific male structures. Post-hoc arguments invoking possible coevolution of defensive female behavior instead of morphology, or of female sensitivities and responses to male sensory traps, could enable the sexually antagonistic coevolution hypothesis to explain these data. No case of such coevolution of female behavior or sensitivities has been demonstrated, and there are additional reasons to doubt that they are general explanations for the data presented here. Detailed studies of female resistance behavior could help illuminate several issues. The possibility of a greater role for antagonistic coevolution in reproductive physiology than in morphology and the possibility that female choice and sexually antagonistic coevolution have both been important in some lineages are discussed.

Male-female conflict and genitalia: failure to confirm predictions in insects and spiders.

Some recent models suggest a new role for evolutionary arms races between males and females in sexual selection. Female resistance to males is proposed to be driven by the direct advantage to the female of avoiding male-imposed reductions in the number of offspring she can produce, rather than by the indirect advantage of selecting among possible sires for her offspring, as in some traditional models of sexual selection by female choice. This article uses the massive but hitherto under-utilized taxonomic literature on genitalic evolution to test, in a two-step process, whether such new models of arms races between males and females have been responsible for rapid divergent evolution of male genitalia. The test revolves around the prediction that 'new arms races' are less likely to occur in species in which females are largely or completely protected from unwanted sexual attentions from males (e.g. species which mate in leks or in male swarms, in which males attract females from a distance, or in which females initiate contact by attracting males from a distance). The multiple possible mechanical functions of male genitalia are summarized, and functions of male genitalic structures in 43 species in 21 families of Diptera are compiled. Functions associated with intromission and insemination (e.g. seizing and positioning the female appropriately, pushing past possible barriers within the female, orienting within the female to achieve sperm transfer), which are unlikely to be involved in new arms races when females are protected, are shown to be common (> 50 % of documented cases). This information is then used to generate the new arms race prediction: differences in genitalic form among congeneric species in which females are protected should be less common than differences among congeneric species in which females are vulnerable to harassment by males. This prediction was tested using a sample of 361 genera of insects and spiders. The prediction clearly failed, even when the data were adjusted to take into account several possible biases. Comparative analyses within particular taxonomic groups also failed to show the predicted trends, as did less extensive data on other non-genitalic male display traits. Arms races, as defined in some recent models, seem to have been less important in male-female coevolution of genitalic structures than has been suggested. By elimination, alternative interpretations, such as traditional female choice, which do not predict associations between female protection from harassment and rapid divergent evolution, are strengthened.