Stifled sex in sympatry: patterns of sexual incompatibility among desmognathine salamanders

Sexual incompatibility due to differences in mate-recognition systems can be an important factor in preventing hybridization and gene flow between animal populations in sympatry. We tested in the laboratory for sexual incompatibility between populations of two species of desmognathine salamanders that occur in sympatry in south-eastern Kentucky, North America, Desmognathus monticola and D. welteri (Caudata: Plethodontidae: Desmognathinae). Spermatophore deposition and insemination (two related measures of sexual success) were frequent in intraspecific encounters, but interspecific encounters never resulted in the deposition of spermatophores by males (Experiment 1). The sexual behaviour patterns of these two species are similar qualitatively, but all encounters staged between them failed to progress beyond the most preliminary of courtship interactions (Experiment 2), perhaps due to species differences in chemosensory communication. Our data on sexual incompatibility between D. monticola and D. welteri are similar to those available for other desmognathine taxa that occur in sympatry. Review of a broader data-set on patterns of sexual incompatibility both within and between species, and in allopatry and in sympatry, provides evidence for both divergence of mate-recognition systems in allopatry and enhancement of sexual incompatibility in sympatry for desmognathine salamanders. We hypothesize that diversification in allopatry may be a consequence of natural and/or sexual selection acting to promote sexual success within populations. Enhancement in sympatry may be a consequence of subsequent selection for accurate species recognition under the threat of hybridization or gene flow between species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 367–375.     

Evolution of Courtship Behaviour Patterns and Reproductive Isolation in the Desmognathus ochrophaeus Complex

The extent to which differences in courtship behaviour patterns act as mechanisms of reproductive isolation is critical to understanding both speciation and the evolution of these behaviour patterns. While numerous studies have investigated intraspecific and interspecific differences in courtship, fewer interpret results in a phylogenetic framework. We describe and analyse geographic variation in the courtship behaviour patterns of the Allegheny Dusky salamander ( Desmognathus ochrophaeus ). We then examine courtship among closely related species in the D. ochrophaeus complex in a phylogenetic context. We found that populations of D. ochrophaeus separated by extensive geographic distances show little variation in courtship behaviour patterns and are sexually compatible. This contrasts with significant levels of sexual isolation between D. ochrophaeus and other species in the complex. Mapping behaviour patterns onto a phylogeny that we generated from cytochrome b sequences indicates that two behaviour patterns present in the courtship sequence of other members in the complex have either been lost in D. ochrophaeus or gained independently in other species in the complex. Loss of these behaviour patterns may result in reproductive isolation between D. ochrophaeus and its sister taxon, D. orestes .     

Population and Species Divergence of Chemical Cues that Influence Male Recognition of Females in Desmognathine Salamanders

Growing evidence indicates that males may be more discriminating of mating partners than often has been assumed. In the North American Ocoee dusky salamander, Desmognathus ocoee (Plethodontidae: Desmognathinae), sexual incompatibility among conspecific populations is high in encounters staged in the laboratory, at least in part because males fail to recognize ‘other’ females as appropriate targets for courtship. I used Y-mazes to test the hypothesis that males of D. ocoee discriminate between substrate-borne chemical cues produced by ‘own’ (homotypic) and ‘other’ (heterotypic) females. Males of four populations discriminated in favor of substrates soiled by homotypic females over clean (control) substrates (expt 1), suggesting that females produce chemical cues of sociosexual significance to males. Furthermore, males from these populations discriminated in favor of substrates soiled by homotypic females vs. substrates soiled by heterotypic females (expt 2), both conspecific and heterospecific (D. carolinensis and D. orestes). Thus, differences among populations and species in female chemical cues appear to affect the chemotactic responses of males. I suggest that, together with differences in behavioral signals and responses exhibited during courtship, differences in female chemical cues likely contribute to sexual incompatibility among populations and taxa of desmognathine salamanders.     

Agonistic and courtship behaviour patterns in the skink Chalcides viridanus (Fam. Scincidae) from Tenerife

There have been relatively few attempts to quantitatively describe behaviours in scincid lizards. Chalcides viridanus is a small body-sized skink endemic of Tenerife (Canary Islands). We describe and quantify 18 behaviour patterns (both social and agonistic) of this species, some of which have not been described before for other scincids. Video recordings of male–male, female–female, and male–female interactions were made under laboratory conditions, with controlled light–dark cycle and temperature. We describe several agonistic and courtship behaviour patterns. Within the first context, we detected a new agonistic behaviour for a scincid, “Snout to body”, that appeared at the beginning of agonistic sequences; it consisted of each animal placing its snout in contact with the other individual’s lateral side of the body. The amplitude of head movement during “Head bobbing” was lower than that described for many other lizard species. Agonistic behaviours were shown in intrasexual staged encounters both within males and females. The comparison of behaviour patterns of both types of intrasexual encounters showed that females were more active, exhibiting significantly higher frequencies of behaviour than males. Specifically, females showed the “Snout to body” pattern more frequently than males. In male–female encounters we detected courtship and copulation patterns only in April, when males performed “Bites” and “Snout to body” directed at females.     

The courtship behaviour of the spotted dusky salamander, Desmognathus fuscus conanti (Amphibia: Caudata: Plethodontidae)

The courtship behaviour of the North American southern dusky salamander, Desmognathus fuscus conanti (Plethodontidae), is described for the first time. The male is the most active participant, as is typical for caudate amphibians, and much of his behaviour can be understood in terms of orientation to and stimulation (or persuasion) of the female. The latter is largely accomplished by the transfer of courtship pheromones from the male's mental (chin) gland. The orientation and persuasion phases of courtship appear necessary if sperm transfer by means of a spermatophore deposited upon the substratum is to be successful. The courtship of D. fuscus conanti is qualitatively identical to that of D. santeetlah , with which it is sexually compatible in the laboratory and with which it may hybridize in nature. However, a broader comparison of species in the genus Desmognathus reveals that the greatest interspecific differences occur during the orientation and persuasion phases of courtship. A complete understanding of the evolution of courtship behaviour in desmognathine salamanders awaits availability of ethograms for all other taxa and a robust, independent phytogeny for the entire subfamily.     

Sexual behaviour of Anastrepha obliqua (Macquart) (Diptera: Tephritidae): Do laboratory domestication conditions influence male courtship behaviour?

We analysed the influence of laboratory domestication, under relaxed conditions, on the courtship behaviour of the fruit fly species Anastrepha obliqua, an important agricultural pest. We compared the temporal patterns of pheromone emission (Calling behaviour) and the frequencies and sequences of the courtship behavioural units of males of a laboratory lineage and a wild lineage. Our results indicated similarities in the temporal behavioural patterns of calling, the durations of their behavioural sequences, the final sequences of courtships resulting in copulation, of wild and laboratory males. Differences, however, were observed between the two populations in terms of the frequencies of the behavioural units executed and the initial sequence of courtship. Differences were noted in the presence or absence of some behavioural units within the courtship behavioural repertoires of the laboratory-reared and wild. The wild males did not show units such as Alignment, Contact, Fighting and Marking Leaf that were observed in the laboratory males' courtship behaviour under laboratory conditions; on the other hand, laboratory males did not show the Abdominal movements and Oscillation observed in the courtship behaviour of wild males. The rearing of A. obliqua males under relaxed conditions in the laboratory provides an environment adequate for the preservation of behavioural characteristics relevant to the successful mating, such as Movement, Arrowhead 1, and Attempt, and in temporal patterns of pheromone emission.     

A Comparative Study of the Behaviour of Six Taxa of Male and Female Gerbils (Rodentia) in Intra- and Interspecific Encounters

Frequencies and sequences of visually-identifiable acts were investigated in male-female combinations of gerbils of the taxa Tatera brantsii, Gerbillurus paeba paeba, G. p. exilis, G. tytonis, G. setzeri, and G. vallinus. Sexual dimorphism of behaviour was most apparent in T. brantsii, G. setzeri, and G. vallinus, in which following, anogenital sniffing, and mounting were significantly more frequently performed by males than females. Females of all taxa presented and darted, while males did not perform these acts. Analysis of first-order transitions of acts in intraspecific encounters revealed remarkable similarity among species in the sequences identified as most significantly deviating from expected frequency. Species-specific patterns of behaviour were detected by discriminant analysis. G. p. paeba, G. p. exilis and G. vallinus were not clearly distinguished by discriminant analysis, and presented a behaviour pattern characterized by low levels of aggression and high levels of huddling behaviour. G. tytonis, G. setzeri and T. brantsii were characterized by low levels of huddling, G. tytonis performed the largest number of upright postures of all taxa, G. setzeri watched more than other taxa, and T. brantsii nasal sniffed less frequently than Gerbillurus taxa. Differences among taxa were more apparent in males than in females. Interspecific encounters were staged between G. p. paeba and G. p. exilis, G. p. paeba and G. tytonis, G. setzeri and G. vallinus. Males showed more evidence of changed behaviour in interspecific encounters than females. More sexual and less agonistic behaviour was detected in intraspecific encounters than in interspecific encounters, but this was statistically significant in only 5 of 12 combinations. Visual, tactile and olfactory communication during physical contact with another individual may complement auditory communication in promoting conspecific recognition in southern African gerbils.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

Male—male aggression in the plethodontid salamander Desmognathus ochrophaeus

Aggressive encounters between pairs of male mountain dusky salamanders (Desmognathus ochrophaeus) were staged in the laboratory in the absence of any obvious limited resource. We observed aggressive interactions which sometimes escalated to biting. Physical injuries were inflicted during some aggressive encounters; however, the consequences of injury for future fitness are uncertain. Several behaviour patterns used in contests apparently functioned as threat displays, and these sometimes ended contests before they escalated to biting. We could detect no significant influences of three types of asymmetries among males in determining the winners and losers of contests (body size, recent mating experience and familiarity with the testing arena). Three cases of 'homosexual' courtship were observed. Both intermale aggression and intermale courtship may be interpreted as forms of competition for mates.     

Male displays and female preferences in the courtship of a gregarious cricket

The courtship of males of the gregarious cricket Amphiacusta maya involves a variety of signals. The quantitative aspects of both successful and unsuccessful courtship sequences were examined to determine whether certain aspects of male displays were correlated with female mating preferences regardless of which male performed them. Although variability among males was high for most courtship components measured, I found no evidence of female choice with respect to the courtship variables studied. About 35% of the duration of each male courtship sequence is devoted to chirping, but there were no differences in either the likelihood of copulation or the latency to copulation between normal males and experimentally silenced males. The possibility that intrinsic differences in male quality explained the variability in courtship duration was examined with a two-way analysis of variance. The variance in courtship duration was attributable to variance among females, not to variance among males. Thus the courtship behaviour of male A. maya is variable enough to allow females to exert stabilizing or disruptive selection on displays, but there is no evidence that females use the available information.     

Courtship versatility in the jumping spider, Phidippus johnsoni (Araneae: Salticidae)

A given male of P. johnsoni has at his disposal two alternative types of courtship. Each consists of distinctly different motor patterns and involves different sensory channels. If the male encounters a female outside her nest, he uses type 1 courtship. Type 2 courtship occurs if the male encounters a female inside her nest. Spiders do not respond to visual stimuli (house flies) under red light. The fact that type 2, but not type 1, courtship occurs when spiders are observed under red light is taken as evidence that type 1 is vision dependent, whereas type 2 is not vision dependent. Selection factors favouring the evolution of courtship versatility are discussed.     

A Comparative Analysis of Mating Recognition Signals in Graylings: Hipparchia statilinus vs. H. semele (Lepidoptera: Nymphalidae, Satyrinae)

Courtship is an important character linked to fitness and can evolve in response to female mate choice, to ensure sex identity and quality of a potential mate. It can also be a major pre-mating isolating mechanism in butterflies and many other species. In this paper, aspects of the reproductive behaviour of Hipparchia statilinus are described. First, the ethogram and the sequential structure of courtship leading to copulation and female refusal behaviour are showed; second, the results are compared with the behaviour of the sympatric and syntopic species, H. semele. Sequential analysis of H. statilinus courtship showed that, once a male has started the sequence, the following steps most likely follow up to the end. Courtship seems to reflect female behaviour: the male can repeat the whole sequence or part of it more than once, waiting for female signals. The general pattern of sexual behaviour in H. semele and in H. statilinus is mainly identical: perching strategy, flight pursuit, courtship. In both species, courtship consists of a highly stereotypic sequence, and differences between sequences are primarily related to presence/absence, order and performance of steps. This study is the first step of an experimental design addressed to a better understanding of mating recognition signals in Hipparchia and provides more details to define the relative roles of phylogeny and environment in shaping boundaries among species.     

Sexual Interference in the Sword-tailed Newt,Cynops ensicauda popei (Amphibia: Salamandridae)

This paper describes competitive interaction between males of the salamandrid Cynops ensicauda popei. The sexual behaviour of the male is influenced by the presence of a second, rival, male. Competition for access to the female and other male interactions continuously interrupt ongoing courtships. Spermatophore pick-up success is lower than in encounters involving single pairs. During triad encounters, fewer spermatophores were deposited than in dyad encounters, due to interference during the creep stage of courtship. Two basic forms of male sexual interference were distinguished: ‘lure away’ during the creeping stage, from a position that is different from the direction of creep; and ‘female mimicry’, during which the male presses his snout alternately against the courting male's tail and the female's snout. In both forms, a rival male may shove one of the courting individuals away. The repertoire of sexual behaviour patterns of Cynops ensicauda popei appears to be less complex and varied than that of most Triturus species. The courtship of Cynops places less emphasis on display behaviour with tail and body, and a stronger emphasis on the creeping stage, where the male carefully leads the responsive female over a series of spermatophores, but during which rival males may interfere in a variety of ways.     

Identified descending brain neurons control different stridulatory motor patterns in an acridid grasshopper

During courtship sequences male grasshoppers of the species Omocestus viridulus successively perform with their hindlegs three different stridulatory movement patterns: ordinary stridulation, hindleg shaking and precopulatory movements. Microinjection of acetylcholine into protocerebral neuropil regions can either elicit complete courtship sequences or evoke one of the three motor patterns. Intracellular recordings and stainings revealed three types of descending brain neurons: B-DC-3, B-DC-4 and B-DC-5. All three types of interneurons have a medial axon position in the connectives. They cross the midline of the protocerebrum and exhibit a profuse arborization pattern within the medial dorsal protocerebral neuropil. Stimulation of each type of interneuron specifically elicits one particular motor pattern of courtship behaviour. Courtship of the grasshopper O. viridulus may therefore be controlled by successive activation of these descending brain neurons. Accepted: 27 September 1996     

Effects of group stability, male-male aggression, and male courtship behaviour on environmentally-induced ovarian recrudescence in the lizard Anolis carolinensis

Reproductively inactive, winter dormant female Anolis carolinensis were exposed to a stimulatory environmental regime while in socially stable or unstable male-female groups. In a second experiment, winter dormant females were exposed to varying amounts of male courtship and male-male aggression. Results indicate that (1) the presence of a stable dominance hierarchy among group males is necessary for male facilitation of environmentally-induced ovarian recrudescence (OR) (an unstable dominance hierarchy inhibits OR), (2) the behaviour patterns responsible for the facilitation and inhibition of environmentally-induced OR are courtship and male-male aggression, respectively, and (3) ovarian development is graded in accordance to the amount of male courtship to which the female is exposed. It is proposed that male courtship insures normal gonadotropin (GT) secretion while the absence of male courtship results in subnormal GT secretion and the presence of male-male aggression suppresses environmentally-induced GT secretions. The functional significance of the inhibition of environmentally-induced OR by male-male aggression and its possible relation to differential vernal emergence in temperate-zone reptiles is discussed.     

Social and maintenance behaviour in two Australian ocypodid crabs (Crustacea: Brachyura)

The feeding, burrowing and fighting behaviour and courtship display of the two ocypodids Heloecius cordiformis (H. Milne Edwards) and Hemiplax latifrons (Haswell) are described from daytime observations in the field over a two-year period and from four months study under laboratory conditions. The behaviour of the two species is compared with that of other ocypodid crabs. Heloecius cordiformis and Hemiplax latifrons live intertidally in estuaries in semi-permanent burrows and feed on detritus sifted from the mud and sand by the mouth-parts. The two species each possess considerably stereotyped patterns of behaviour, particularly in relation to fighting and courtship display in which the two differ most. The courtship display of Heloecius cordiformis closely resembles that of vertically waving, narrow-fronted species of fiddler crabs (genus Uca). The fighting behaviour of Hemiplax latifrons is similar to that of the New Zealand Hemiplax hirtipes (Jacquinot) which apparently lacks courtship display.     

Aggressive behaviour and dominance relationships of the dark chub,Zacco temmincki with special reference to their individual recognition

Aggressive behaviour and dominance relationships ofZacco temmincki were observed by introducing fish into an enclosed pond. Chase (-flee), lateral display, parallel swim and butt were the principal behavioural patterns in aggressive encounters between fish, while chase, resulting in lateral display by the chased fish was the most common behavioural sequence. Initially, mutual behavioural patterns such as parallel swim and mutual lateral display were most evident among the total aggressive acts although chase became dominant three days after introduction into the pond. The dominance matrix constructed from chase-flee interactions during all observation periods contained many reverse attacks (336 out of 2,740 chases). These reverse attacks did not concentrate upon a specific period and were not site-dependent. Examination of chase-flee interactions and the subsequent behavioural pattern revealed that a chased fish reacted to the chaser either by attacking in turn, or performing lateral display etc. roughly in relation to the dominance rank of the chaser. This result implies that fish recognized each other to a great extent during aggressive encounters. It seems likely that such individual recognition was initiated during the early period when mutual behaviour was most frequent, and that some attacks against the dominance order were caused as a result of revolts rather than mistakes.     

Conditional strategies and interpopulation variation in the behaviour of jumping spiders

Abstract

Conditional strategies and interpopulation variation in the mating and predatory behaviour of salticid spiders are reviewed. A functional approach is adopted, and defended, in which specified behavioural phenotypes are accounted for, in large part, by specified selection factors. Courtship versatility, in which a male's behaviour depends on the female's maturity and location, is common in the Salticidae. If a male encounters an adult female in the open, where there is ample ambient light, he performs vision-dependent displays (Type 1 courtship) in front of her. If he encounters an adult female inside her nest, he uses different displays (Type 2 courtship) which are not vision–dependent and consist of various tugging, probing and jerking movements on the silk of the nest. These displays apparently send vibratory stimuli to the female. When a male encounters a subadult female inside her nest, he initially performs Type 2 courtship, then spins a second chamber on the nest and cohabits until the female moults and matures. A modification of optimal foraging theory has been used to examine factors that influence interpopulation variation in male courtship persistence. A study of five populations corroborated predictions from the model. Persistence appears to be related to female availability. Female availability is related to local phenology, which is, in turn, related to local climate. Complex examples of predatory versatility also have evolved in the Salticidae, especially in the genus Portia. All species of Portia studied are araneophagic spiders that invade other spiders' webs and practise aggressive mimicry. Portia fimbriata, uniquely among Portia species studied, uses specialised behaviour to prey on other salticids. Portia fimbriata and one of the salticids on which it preys, Euryattus sp., appear to be co-adapted to each other.     

Reproductive barriers between the partially sympatric Colorado and false potato beetles

The partially sympatric Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say), and the false potato beetle (FPB), Leptinotarsa juncta (Germar), were shown to possess a series of reproductive barriers that protect species integrity. A strongly stereotyped sequence of courtship behaviour insures that more than 85% of encounters between these congeneric species are terminated before copulation. The courtship behaviour of the FPB, described here for the first time, is similar to that for the CPB. However, the male FPB is more likely to walk off the female FPB and will repeat antennal tapping more frequently than the CPB before moving on to palp tapping and mating. Observations suggest that both species first use antennal tapping for an initial olfactory assessment of the object as a female insect of a given family or species and palp tapping for final sex recognition. If courtship behaviour fails to break up the hybridization pairs, there is no mechanical barrier to mating and sperm transfer takes place. However, there is gametic mortality. The FPB is more fecund than the CPB and seems less dependent than the CPB on multiple matings to reach its full reproductive potential.