Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.     

Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat

One of the great mysteries of coral-reef fish ecology is how larvae locate the relatively rare patches of coral-reef habitat on which they settle. The present study aimed to estimate, by experiments in aquaria, the sensory modalities of coral-reef fish larvae for senses used in searching for their species settlement habitat. Larval recognition of settlement habitat can be based on the detection of conspecifics and/or of characteristics of coral habitat using visual, chemical and mechanical cues. For this study, larvae were captured with crest nets and were then introduced into experimental tanks that allowed testing of each type of cue separately (visual, chemical or mechanical cues). Among the 18 species studied, 13 chose their settlement habitat due to the presence of conspecifics and not based on the characteristics of coral habitat, and 5 species did not move toward their settlement habitat (e.g. Scorpaenodes parvipinnis, Apogon novemfasciatus). Among the different sensory cues tested, two species used the three types of cues (Parupeneus barberinus and Ctenochaetus striatus: visual, chemical and mechanical cues), six used two types (e.g. Myripristis pralinia: visual and chemical cues; Naso unicornis: visual and mechanical cues), and five used one type (e.g. Chrysiptera leucopoma: visual cues; Pomacentrus pavo: chemical cues). These results demonstrate that many coral-reef fish larvae could in practice use sensory cues for effective habitat selection at settlement, and have the ability to discriminate species-specific sensory cues.Communicated by J. Krause     

Individual and species recognition in centrarchid fishes: evidence and hypotheses

Summary We conducted laboratory experiments to determine if juveniles of three species of centrarchid fishes displayed abilities for species or individual recognition. In one experiment we reared rock bass (Ambloplites rupestris) in social isolation and in social groups. Both the isolated and group-reared fish spent significantly more time close to conspecifics than to heterospecifics. These results suggest that species recognition in rock bass is controlled by a closed genetic program and that social experience is not necessary. A second set of experiments was conducted to determine if year-old blue-gill (Lepomis macrochirus), pumpkinseed (L. gibbosus), and rock bass juveniles could discriminate between familiar and unfamiliar conspecifics. Bluegill spent significantly more time with familiar conspecifics than with unfamiliar conspecifics, while the other two species displayed no such trend. Bluegill spent significantly more time with familiar conspecifics than did either of the other two species. We postulate that these interspecific differences in recognition abilities may be related to differences in habitat and group parameters among the species.     

Social experience during adolescence influences how male zebra finches (Taeniopygia guttata) group with conspecifics

Group-living animals rely on social skills which ensure beneficial interaction and prevent harmful ones with conspecifics. In a previous experiment, we demonstrated that male zebra finches reared in groups during adolescence show consistently less courtship and aggressive behaviour as adults than pair-reared males. Here we tested whether such differences affect how they group with conspecifics, as an indicator of their social integration. Zebra finches were kept in pairs (male–female or male–male) or mixed-sex groups (three males and three females) during adolescence and were introduced to an established group of unknown conspecifics during adulthood. Male courtship and aggressive behaviour were quantified directly after introduction to the group and 48 h later. At the same time, male position in relation to other birds and the number of birds in proximity were recorded. Males that grew up in a small mixed-sex group during adolescence spent more time within groups, were observed in bigger groups and lost less weight than males raised in pairs, indicating that an enriched social environment during early development may facilitate social integration. However, we observed no differences in courtship and aggressive behaviour that could predict the differences in grouping behaviour of pair- and group-reared males. We discuss alternative explanations for the difference in grouping and how to test these in future research.     

Shoaling fish can size-assort by chemical cues alone

Animals that form groups are typically assorted by phenotype. For example, fish shoals are notably composed of closely size-matched individuals, yet the sensory mechanisms that promote this behaviour have not been fully determined. Here, we show that two freshwater shoaling fish species, three-spined stickleback and banded killifish, have a greater preference for the chemical cues of conspecifics that are the same size as themselves than for those of larger or smaller conspecifics. We suggest that this ability to determine their own size relative to conspecifics may be based on chemical self-referencing. This provides a novel insight to the mechanisms underlying a widespread phenomenon in social behaviour, and provides further evidence of the crucial role played by chemical cues in structuring the interactions of fishes.     

Asexuals looking for sex: conflict between species and mate-quality recognition in sailfin mollies (Poecilia latipinna)

When two closely related species are sympatric the process of species recognition (identifying conspecifics) and mate-quality recognition (increased fitness benefits) can yield a conflict when heterospecifics resemble high-quality conspecifics. Conflict in species versus mate-quality recognition may serve as a possible mechanism for the persistence of unisexual, gynogenetic Amazon mollies (Poecilia formosa). Amazon mollies require sperm from closely related species (e.g., sailfin mollies, P. latipinna) to start embryogenesis but inheritance is strictly maternal. When choosing mates, male sailfin mollies from populations sympatric with Amazon mollies may rely on traits indicating species identity rather than those indicating mate quality. Conversely, males from allopatric populations may rely more on traits indicating mate quality. Previous work has found that male sailfin mollies in sympatry exhibit a significantly greater mating preference for female sailfin mollies over Amazon mollies compared to males in allopatry. In addition, male sailfin mollies prefer to associate with and produce more sperm in the presence of larger conspecific females, which are more fecund. We hypothesized that male sailfin mollies experience a conflict in species recognition and mate-quality recognition in the presence of Amazon mollies that are relatively larger than female sailfin mollies. To test this hypothesis, we paired males from sympatric and allopatric populations with a larger Amazon molly and a smaller female sailfin molly. We scored the number of mating attempts that males directed to conspecific and heterospecific females. Males in most sympatric and allopatric populations demonstrate no clear preference for conspecifics. In addition, we found some evidence for a difference in mating preference between allopatric and sympatric populations with males from allopatry showing a greater heterospecific mate preference. These results indicate a conflict between species and mate-quality recognition. In sympatry this conflict may contribute to the persistence of gynogenetic Amazon mollies.     

A test of the senses: fish select novel habitats by responding to multiple cues

Habitat-specific cues play an important role in orientation for animals that move through a mosaic of habitats. Environmental cues can be imprinted upon during early life stages to guide later return to adult habitats, yet many species must orient toward suitable habitats without previous experience of the habitat. It is hypothesized that multiple sensory cues may enable animals to differentiate between habitats in a sequential order relevant to the spatial scales over which the different types of information are conveyed, but previous research, especially for marine organisms, has mainly focused on the use of single cues in isolation. In this study, we investigated novel habitat selection through the use of three different sensory modalities (hearing, vision, and olfaction). Our model species, the French grunt, Haemulon flavolineatum, is a mangrove/seagrass-associated reef fish species that makes several habitat transitions during early life. Using several in situ and ex situ experiments, we tested the response of fish toward auditory, olfactory, and visual cues from four different habitats (seagrass beds, mangroves, rubble, and coral reef). We identified receptivity to multiple sensory cues during the same life phase, and found that different cues induced different reactions toward the same habitat. For example, early-juvenile fish only responded to sound from coral reefs and to chemical cues from mangroves/seagrass beds, while visual cues of conspecifics overruled olfactory cues from mangrove/seagrass water. Mapping these preferences to the ecology of ontogenetic movements, our results suggest sequential cue use would indeed aid successful orientation to novel key habitats in early life.     

Behavioral and electroantennographic responsiveness of adult butterflies of six nymphalid species to food-derived volatiles

While adults of most species of butterflies visit flowers for food (nectar), those of certain species can feed on rotting food (e.g., exuded tree sap and rotting fruits). These food sources considerably differ in odor; flowers emit species-specific scents and rotting-food odors are characterized by fermentation products. To determine whether adult butterflies have different olfactory performances adaptive to their food selections, we examined the following responses of naïve adults of six nymphalid species, namely, Nymphalis xanthomelas, Kaniska canace, Vanessa indica, Cynthia cardui, Hypolimnas bolina, and Argyreus hyperbius: the proboscis extension reflex (PER) was evaluated as the behavioral criterion of preference for scent compounds, and the electroantennographic (EAG) response was assessed as the sensory criterion of antennal perception. All of these species are nectarivorous, but N. xanthomelas, K. canace, and V. indica also forage rotting food. The PERs to 52 tested compounds were in good agreement with the food habits of these butterflies. The six species showed high PERs to several aromatic compounds widely found in flower scents. Fermentation products such as ethanol and acetic acid elicited intermediate to high responses from the three species feeding on rotting foods. The other three species showed low PERs to these compounds, and acetic acid strongly inhibited the PER-eliciting activities of the other compounds. These results demonstrate that the olfactory preference for fermentation products is a characteristic of the rotting-food feeders. The spectrum of EAG responses to 37 tested compounds was relatively similar among the six species. Particular acyclic aliphatic compounds, including green leaf volatiles, elicited high EAG responses from all the species. Despite a high PER-eliciting activity, most aromatic compounds induced intermediate EAG responses; however, ethanol and acetic acid evoked very weak responses. The results suggest that in food selection, adult butterflies use a specific olfactory system to perceive these major food-derived volatiles.     

Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations.

When breeding diet is restricted, domesticated zebra finches,Taeniopygia guttata, produce male-biased primary and secondary sex ratios, but unexpectedly produce unbiased ratios when food is unrestricted. We investigated the primary sex ratios (at laying) of wild zebra finches in southeastern Australia in response to food supplementation and environmental factors predicted to enhance female breeding condition and to bias the primary sex ratio towards daughters. Molecular sexing of all nestlings in 54 complete broods where every egg hatched, failed to show any significant biases from random. Time of egg laying (month, season) and environmental conditions (rainfall, temperature) did not significantly predict variation in the primary sex ratio, but time of breeding did affect clutch size. Wild zebra finches at our colony did not bias their sex allocation as there were no differences in the primary sex ratio and no differences in the numbers and mass of sons and daughters at the end of parental care (day 35–40 post-hatch). Biases in primary sex ratio of our wild population are probably weak or non-existent possibly due to the unpredictable environment and/or multiple contrary selective forces acting on sex ratios. We also investigated the effects of photoperiod, biases in the adult sex ratio, and parental attractiveness on primary sex ratios of semi-domesticated, laboratory zebra finches. Molecular sexing of three-day old embryos from complete clutches, failed to reveal significant biases from random. In contrast to previous studies, sex of eggs did not correlate with laying order and egg mass declined with order, rather than increased. Domestication may be responsible for these differences.     

Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice

The mechanisms and functions of mixed-species shoaling were investigated in two sympatric species of cyprinids, the chub and the European minnow, from the river Wharfe where they comprised approximately 70% of all year 0+ fish over a 20-year survey. Chub preferred conspecific shoals over heterospecific ones with olfactory cues being more important than visual ones for shoal choice. This preference was consistent with measurements of length:flank area ratios and length:weight ratios which suggest that both species are similar in appearance. When presented with mixed-species shoals, chub increased the percentage time spent with stimulus shoals with increasing proportions of conspecifics. Feeding experiments suggest that the preference for conspecific shoals is driven by interspecific competition (with minnows out-competing similar-sized chub) and the oddity effect. The importance of this work in the context of species assortment in free-ranging shoals is discussed.     

Kin recognition in the common lizard

The ability to recognize parents has never been reported in species in which parents do not provide care to their young; in such species, only sibling recognition has been found. However, there may be several advantages of parent recognition, even in the absence of parental care. We investigated the ability of neonates to recognize olfactory cues from both their mother and siblings in the common lizard, Lacerta vivipara, a species without parental care. Juveniles from 264 gravid females were reared for 2 days either with their mother, with another female, or separated from all other adults. Juveniles from some families were split into two or three groups so that each juvenile was unfamiliar with a subset of its siblings. After 2 days, we offered the juveniles a choice of two nocturnal shelters: one containing a lizard odor and the other without odor. The response to the odor of an unrelated and unfamiliar adult was influenced by both the sex of the adult and the sex of the juvenile. Juveniles of both sexes recognized the odor of their mother whether they were familiar with her or not (pre-natal determinism). Juveniles recognized familiar but not unfamiliar siblings (post-natal determinism). In the wild, spatial association with kin declines shortly after birth. Thus, recognition of the mother is likely to have biological relevance. Recognition of the mother may reduce competition and/or enhance juvenile establishment. Received: 15 May 1997 / Accepted after revision: 29 December 1997     

No cultural transmission of species recognition between parents and offspring in free-living great tits and blue tits

Imprinting plays a key role in the development of species recognition, with young imprinting upon the morphological characters of their parents. However, the potential role that cultural transmission might play in species recognition remains largely uninvestigated. Great tits (Parus major) and blue tits (Cyanistes caeruleus) do not normally perceive each other as sexual competitors or potential partners. However, after reciprocal interspecific cross-fostering, both species may perceive individuals of the foster species as potential rivals or mates. Although the experience of being raised by heterospecifics clearly has affected the species recognition of cross-fostered birds, some of them breed naturally with conspecifics. The offspring of such cross-fostered birds (OCF) are hence raised by parents that look like ordinary conspecifics but display deviant species recognition as compared to controls in terms of aggressive response towards rivals. Comparing the aggressive behavior of OCF, cross-fostered birds and controls towards territorial intruders may thus help tease apart the influence of morphological vs behavioral cues of parents in the development of offspring species recognition. To this end, we compared birds from all three treatments with respect to their aggressive response to territorial intruders of both species during the breeding season. OCF and controls did not differ in their pattern of response towards heterospecific and conspecific stimuli. Compared to cross-fostered birds, OCF and controls showed less aggression towards heterospecific intruders, while the response towards conspecific intruders did not differ between treatments. These results demonstrate that both tit species imprint on the morphological characters of their parents, but that parental behavior is not important for the development of species recognition in terms of aggressive response towards territorial intruders.     

Chemical communication in green and golden bell frogs: do tadpoles respond to chemical cues from dead conspecifics?

Captive bred animals often lack the ability of predator recognition and predation is one of the strongest causes of failure of breed and release projects. Several tadpole and fish species respond defensively to chemical cues from injured or dead conspecifics, often referred to as alarm pheromones. In natural conditions and in species that school, the association of chemical cues from predators to alarm pheromones released by attacked conspecifics may lead to the learning of the predator-related danger without experiencing an attack. In the laboratory, this chemical communication can also be used in associative learning techniques to teach naïve tadpoles to avoid specific predators and improve survivorship of released animals. In our experimental trials, tadpoles of the threatened green and golden bell frog (Litoria aurea) did not avoid or decrease their activity when exposed to solutions of conspecific macerate, suggesting that the chemicals released into the water by dead/injured conspecifics do not function as an alarm pheromone. This non-avoidance of dead conspecific chemicals may explain why green and golden bell frog tadpoles have seemingly not developed any avoidance behaviour to the presence of introduced mosquito fish, and may render attempts to teach naïve tadpoles to avoid this novel predator more difficult.     

Mate-choice copying by female zebra finches, <Emphasis Type="Italic">Taeniopygia guttata</Emphasis>: what happens when model females provide inconsistent information?

For a long time, mate-choice copying was thought to be restricted to lekking and polygynous species. Yet, recent experimental studies revealed that social information can play a role in the evolution of mate preferences in monogamous species with biparental care. However, this phenomenon has been demonstrated only under particular conditions and the prevalence and importance of this phenomenon therefore remains to be evaluated. In particular, previous laboratory experiments have consisted in exposing test females to only one paired male at a time, while under natural conditions monogamous females are likely to observe the choice of several females before making a decision. Thus, in the present study, female zebra finches (Taeniopygia guttata) could observe two model females simultaneously, that provided either inconsistent or consistent information, depending on whether they were interacting with different types of males or with males of a same phenotype. We found that the relative importance given to private and social information on females’ preferences varied with the consistency of social information and females significantly changed their preference only when social information was consistent. There was, nevertheless, a large variation in their responses. We suggest that such variations could be due to the fact that the benefits of mate-choice copying are frequency-dependent, and that this constrain would further contribute to limit the use of social information in monogamous species.     

Mating behavior in three species of Pseudodiaptomus (Copepoda: Calanoida)

Quantitative studies of mating behavior between conspecific and heterospecific pairs of three closely related species in the genus Pseudodiaptomus reveal differences in the timing of life-history events, species-specific attraction of mates, distinctive tactile cues, multiple spermatophore attachments, and gametic incomptibility or hybrid inviability. These differences may function as reproductive isolating mechanisms among calanoid copepods. Differences in breeding behaviors and associated morphological features are greater between sympatric than between allopatric species, indicating that selection reinforces both behavioral and morphological divergences.     

Reduction of the association preference for conspecifics in cave-dwelling Atlantic mollies, Poecilia mexicana

Cave animals are widely recognised as model organisms to study regressive evolutionary processes like the reduction of eyes. In this paper, we report on the regressive evolution of species discrimination in the cave molly, Poecilia mexicana, which, unlike other cave fishes, still has functional eyes. This allowed us to examine the response to both visual and non-visual cues involved in species discrimination. When surface-dwelling females were given a chance to associate with either a conspecific or a swordtail (Xiphophorus hellerii) female, they strongly preferred the conspecific female both when multiple cues and when solely visual cues were available to the female. No association preference was observed when only non-visual cues were provided. In contrast, cave-dwelling females showed no preference under all testing conditions, suggesting that species recognition mechanisms have been reduced. We discuss the role of species discrimination in relation to habitat differences.     

Learned recognition of novel predator odour by convict cichlid embryos

Predation exerts tremendous selection pressure on all organisms. In this study, we exposed embryos of convict cichlids (Amatitlania siquia) twice daily to one of the following: (1) chemical alarm cues of damaged conspecifics + odour of a novel predator (Polypterus endlicheri), (2) chemical alarm cues of damaged conspecifics + water or (3) blank water. No chemical cues were presented after the eggs hatched. When the larvae were 9 days old (mean total length?=?5.7 mm), they were exposed to either predator odour or water. Those larvae that had been conditioned as embryos on alarm cues + predator odour showed a significant reduction in activity (i.e. anti-predator behavioural response) to predator odour relative to the other treatments. This is the first demonstration of acquired predator recognition by fish embryos.     

Odour-based species recognition in two sympatric species of sac-winged bats (<Emphasis Type="Italic">Saccopteryx bilineata,S. leptura)</Emphasis>: combining chemical analyses,behavioural observations and odour preference tests

Combining chemical analysis and odour preference tests, we asked whether two closely related sympatric species of sac-winged bats use odour for species recognition. Males of the two sister species Saccopteryx bilineata and Saccopteryx leptura have pouches containing an odoriferous liquid in their antebrachial wing membrane, which is used in S. bilineata during courtship displays. Although both species occasionally share the same daytime roosts and are morphologically similar, there is no evidence for interbreeding. We compared the production and composition of the wing sac odorant in male S. leptura and S. bilineata and performed odour preference tests with female S. bilineata. Similar to male S. bilineata, male S. leptura cleansed and refilled their wing sacs with secretions, but they spent more time each day in doing so than male S. bilineata. Chemical analysis by gas chromatography and mass spectrometry revealed that male Saccopteryx carried species-specific scents in their wing sacs. Binary choice tests confirmed that female S. bilineata preferred the wing sac scents of male S. bilineata to those of the sister species, suggesting that the species specificity of male wing sac scents maintain the pre-mating isolation barrier between these closely related species.     

“Armpit effect” in an African cichlid fish: self-referent kin recognition in mating decisions of male Pelvicachromis taeniatus

Kin discrimination in nepotistic as well as in sexual contexts is widespread in animals including humans. However, the underlying mechanisms of kin discrimination are assumed to vary between species and—within species—between contexts. During solitary life stages, kin recognition based on social learning is assumed to be less reliable because kin templates that are not continuously updated may get lost. Therefore, self-referent phenotype matching (“armpit effect”), i.e., the comparison of unknown phenotypes with own characteristics, should be particularly relevant when no social cues are available. However, experimental evidence for this mechanism is scarce. Here, we examine self-referent kin recognition in a mate-choice context in adult male Pelvicachromis taeniatus, a socially monogamous cichlid fish from West Africa with biparental brood care and pronounced kin-mating preferences. Juvenile P. taeniatus live in groups, whereas adult males compete for access to breeding sites which they aggressively defend against rivals. Using computer-animated females as standardized visual stimuli in combination with olfactory cues of related and unrelated females, we show that adult males reared isolated from kin since egg stage were able to discriminate sisters from unrelated females. As males could have learned kin cues only from themselves, our study provides evidence for self-referent kin recognition and indicates that the observed inbreeding preferences are mediated by self-derived olfactory cues. Male preferences for sisters were correlated with male body size. We discuss the implications of quality-related mate choice for the evolution of kin-mating preferences.     

Behavioural responses of competent lobster postlarvae to odor plumes

We determined the ability of competent laboratory-reared Homarus americanus postlarvae to use odor plumes as a potential mechanism of orientation during the habitat selection process at settlement. In a Y-maze apparatus, both swimming direction (upstream or downstream) and arm selection (control or experimental) were strongly influenced by the nature of the chemical stimulus tested. In control conditions (unconditioned water in both proximal arms of the experimental device), postlarvae swam predominantly upstream (61:39) but displayed no arm preference (48:52). When submitted to a metabolite solution of adult conspecifics or macroalgae, postlarvae swam consistently upstream (73%) and showed a significant preference for the arm providing these stimuli (69%). In contrast, postlarvae submitted to cunner (Tautogolabrus adspersus) metabolites swam predominantly downstream (68:32), and those that did swim upstream significantly avoided the experimental arm (30:70). In repeated trials with the same individuals, postlarvae behaved similarly in 80% of the assays, suggesting a low intra-individual variability in behavioural responses. It is concluded that distance chemoreception may play a role in habitat selection by lobster postlarvae at settlement.