Studying hybridization is crucial to understanding speciation and almost all our knowledge comes from terrestrial and freshwater environments. Marine hybrids are considered rare, particularly on species-rich coral reefs. Here, we report a significant marine hybrid zone at Christmas and Cocos Islands (eastern Indian Ocean) with 11 hybrid coral reef fishes (across six families); the most recorded hybrids of any marine location. In most cases, at least one of the parent species is rare (less than three individuals per 3000 m2), suggesting that hybridization has occurred because individuals of the rare species have mated with another species owing to a scarcity of conspecific partners. These islands also represent a marine suture zone where many of the hybrids have arisen through interbreeding between Indian and Pacific Ocean species. For these species, it appears that past climate changes allowed species to diverge in allopatry, while recent conditions have facilitated contact and subsequent hybridization at this Indo-Pacific biogeographic border. The discovery of the Christmas–Cocos hybrid zone refutes the notion that hybridization is lacking on coral reefs and provides a natural laboratory for testing the generality of terrestrially derived hybridization theory in the marine environment.
hybridization; Christmas Island; Cocos (Keeling) Islands; suture zone; coral reef fish; phylogeography
Mate choice is mediated by a range of sensory cues, and assortative mating based on these cues can drive reproductive isolation among diverging populations. A specific feature of mormyrid fish, the electric organ discharge (EOD), is used for electrolocation and intraspecific communication. We hypothesized that the EOD also facilitates assortative mating and ultimately promotes prezygotic reproductive isolation in African weakly electric fishes. Our behavioural experiments using live males as well as EOD playback demonstrated that female mate recognition is influenced by EOD signals and that females are attracted to EOD characteristics of conspecific males. The dual function of the EOD for both foraging and social communication (including mate recognition leading to assortative mating) underlines the importance of electric signal differentiation for the divergence of African weakly electric fishes. Thus, the EOD provides an intriguing mechanism promoting trophic divergence and reproductive isolation between two closely related Campylomormyrus species occurring in sympatry in the lower Congo rapids.
assortative mating; Campylomormyrus; electric organ discharge; ecological speciation; weakly electric fish (mormyridae)
Flight-dimorphic insects have been used extensively to study trade-offs between energetically costly traits. Individuals may develop and maintain structures required for flight, or alternatively they may invest in reproduction. Previous experiments have not examined whether flight itself might affect investment into reproduction. As in other Gryllus species, flight-capable individuals of the wing polymorphic cricket, Gryllus texensis, incur an apparent reproductive penalty for being able to fly, expressed as smaller ovaries in females and lower courtship propensity in males, than their flight-incapable counterparts. We find that a short bout of flight eliminates the trade-off. Two days after the flight, the ovaries of flight-capable females were comparable with those of short-winged females. Similarly, flight markedly increased the probability of courtship behaviour. Our results suggest that the impact of the flight–reproduction trade-off described in earlier studies may have been overestimated.
life-history trade-off; flight behaviour; flight dimorphism; wing polymorphism; ovarian development; courtship behaviour
Natural selection plays a fundamental role in the ecological theory of adaptive radiation. A prediction of this theory is the convergent evolution of traits in lineages experiencing similar environments. The Hawaiian honeycreepers are a spectacular example of adaptive radiation and may demonstrate convergence, but uncertainty about phylogenetic relationships within the group has made it difficult to assess such evolutionary patterns. We examine the phylogenetic relationships of the Hawaii creeper (Oreomystis mana), a bird that in a suite of morphological, ecological and behavioural traits closely resembles the Kauai creeper (Oreomystis bairdi), but whose mitochondrial DNA (mtDNA) and osteology suggest a relationship with the amakihis (Hemignathus in part) and akepas (Loxops). We analysed nuclear DNA sequence data from 11 relevant honeycreeper taxa and one outgroup to test whether the character contradiction results from historical hybridization and mtDNA introgression, or convergent evolution. We found no evidence of past hybridization, a phenomenon that remains undocumented in Hawaiian honeycreepers, and confirmed mtDNA and osteological evidence that the Hawaii creeper is most closely related to the amakihis and akepas. Thus, the morphological, ecological and behavioural similarities between the evolutionarily distant Hawaii and Kauai creepers represent an extreme example of convergent evolution and demonstrate how natural selection can lead to repeatable evolutionary outcomes.
ecological convergence; convergent evolution; Hawaiian honeycreepers; mitochondrial DNA introgression; hybridization; adaptive radiation
We report an unusual example of reproductive parasitism in amphibians. Dendrobates variabilis, an Amazonian poison frog, oviposits at the surface of the water in small pools in plants and deposits tadpoles within the pools. Tadpoles are highly cannibalistic and consume young tadpoles if they are accessible. Deposition of embryos and tadpoles in the same pool is common. Genetic analyses indicate that tadpoles are frequently unrelated to embryos in the same pool. A pool choice experiment in the field demonstrated that males carrying tadpoles prefer to place them in pools with embryos, facilitating reproductive parasitism via cannibalism.
reproductive parasitism; egg cannibalism; Dendrobates; Ranitomeya; deposition strategies; anuran
The heat dissipation limit hypothesis suggests that the capacity for lactating mammals to transfer energy to their offspring through milk may be constrained by limits on heat dissipation, particularly in species that raise offspring in well-insulated nests. We tested a prediction of this hypothesis by evaluating whether lactating free-ranging red squirrels (Tamiasciurus hudsonicus) occupy less insulated nests when experiencing conditions that increase heat load. In support of the hypothesis, when climate normal ambient temperatures were warm, squirrels supporting large litter masses of furred offspring occupied nests of lower insulative value. These results support the heat dissipation limit hypothesis and suggest that free-ranging mammals may select nests based on their insulative value, not only to reduce heat loss in cold conditions but also to dissipate heat during periods of heat stress.
endothermy; heat stress; heat dissipation limit hypothesis; parental care
Virulence in pathogens may be increased or decreased in order to maximize reproduction and transmission. We investigated how reproduction and virulence in the entomopathogen Bacillus thuringiensis (Bt) changed with bacterial density. We predicted that virulence would be moderated at high pathogen densities because extended time to death allows more growth in hosts. We found that pathogen reproduction (spores produced per cadaver) peaked at an intermediate time to death and was lowest in hosts that die early. Manipulating spore density (spores per unit area of leaf) by combining pathogenic Bt spores with a non-pathogenic mutant confirmed our prediction: larval 5-day mortality was reduced at higher pathogen densities. Pathogen reproduction increased with the density of pathogenic Bt. We hypothesize that more effective reproduction at high density is a consequence rather than a cause of density-dependent virulence.
Bacillus thuringiensis; mass action theory; prudence; trade-off; tragedy of the commons; quorum sensing
Vocal performance refers to the proficiency with which a bird sings songs that are challenging to produce, and can be measured in simple trilled songs by their deviation from an upper bound regression of frequency bandwidth on trill rate. Here, we show that male swamp sparrows (Melospiza georgiana) increase the vocal performance of individual song types in aggressive contexts by increasing both the trill rate and frequency bandwidth. These results are the first to demonstrate flexible modulation by songbirds of this aspect of vocal performance and are consistent with this signal feature having a role in aggressive communication.
bird song; aggressive signalling; vocal performance
To avoid being captured, prey animals need to be able to distinguish predators from non-predators. Recent studies have shown that amphibians can learn to recognize their future predators while in the egg. Here, we investigated whether amphibians would similarly be able to learn to recognize non-predators while in the egg. We exposed newly laid wood frog eggs to the odour of tiger salamander or a water control daily for 5 days. After hatching, the wood frog larvae were raised for two weeks at which time we tried to condition them to recognize the salamander as a predator. Larvae were exposed to injured conspecific cues paired with salamander odour, a well-established mode of learning for aquatic prey. When subsequently tested for their response to salamander odour, the larvae pre-exposed to water as embryos showed significant anti-predator responses. However, larvae pre-exposed to the salamander odour as embryos showed no learning of the predator, indicating that they had already learned to recognize the salamander as a non-predator. These results indicate that amphibian embryos can (i) learn to recognize stimuli as non-threatening and (ii) remember it for at least two weeks. The widespread ability of prey to learn to recognize non-predators might explain the persistence of injured conspecific cues as a reliable mechanism for learned predator recognition.
predator recognition; latent inhibition; embryo; wood frog Rana sylvatica
Transfers and services are frequent in the animal kingdom. However, there is no clear evidence in animals that such transactions are based on weighing costs and benefits when giving or returning favours and keeping track of them over time (i.e. calculated reciprocity). We tested two orang-utans (Pongo pygmaeus abelii) in a token-exchange paradigm, in which each individual could exchange a token for food with the experimenter but only after first obtaining the token from the other orang-utan. Each orang-utan possessed tokens valuable to their partner but useless to themselves. Both orang-utans actively transferred numerous tokens (mostly partner-valuable) to their partner. One of the orang-utans routinely used gestures to request tokens while the other complied with such requests. Although initially the transfers were biased in one direction, they became more balanced towards the end of the study. Indeed, data on the last three series produced evidence of reciprocity both between and within trials. We observed an increase in the number and complexity of exchanges and alternations. This study is the first experimental demonstration of the occurrence of direct transfers of goods based on calculated reciprocity in non-human-primates.
reciprocal giving; exchange; bartering; economics; primates
Given the high costs of avian obligate brood parasitism, host individuals are selected to reject parasitic eggs they recognize as foreign. We show that rejection may not necessarily follow egg discrimination when selective removal of the parasitic egg is difficult. We studied egg rejection behaviour in a small host of the common cuckoo Cuculus canorus, the eastern olivaceous warbler Hippolais pallida, by experimental parasitism with model and real non-mimetic cuckoo eggs and video recordings of host behaviour. Hosts pecked 87 per cent (20 out of 23) of the model eggs but eventually accepted 43.5 per cent (10 out of 23) of them. A similar pattern was found for real cuckoo eggs, which were all pecked, but as many as 47 per cent (7 out of 15) of them were accepted. To our knowledge, this is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them. Our results also show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoo eggs may avoid rejection by means of their unusually high structural strength.
brood parasitism; egg rejection; cuckoo; olivaceous warbler
The physiological properties of vertebrate skeletal muscle typically show a scaling pattern of slower contractile properties with size. In fishes, the myotomal or swimming muscle reportedly follows this pattern, showing slower muscle activation, relaxation and maximum shortening velocity (Vmax) with an increase in body size. We asked if the muscles involved in suction feeding by fishes would follow the same pattern. We hypothesized that feeding muscles in fishes that feed on evasive prey are under selection to maintain high power output and therefore would not show slower contractile properties with size. To test this, we compared contractile properties in feeding muscles (epaxial and sternohyoideus) and swimming muscle (myotomal) for two members of the family Centrarchidae (sunfish): the bluegill (Lepomis macrochirus) and the largemouth bass (Micropterus salmoides). Consistent with our predictions, the Vmax of myotomal muscle in both species slowed with size, while the epaxials showed no significant change in Vmax with size. In the sternohyoideus, Vmax slowed with size in the bluegill but increased with size in the bass. The results indicate that scaling patterns of contractile properties appear to be more closely tied to muscle function (i.e. locomotion versus feeding) than overall patterns of size.
sunfish; feeding; swimming; scaling
Recent discussion of genetic benefits of polyandry and female mate choice has distinguished between two potential factors influencing offspring quality: (i) some males carry higher quality genes and (ii) males and females differ in their degree of genetic compatibility. We examined evidence for effects of good genes and genetic compatibility on embryonic survival of sea lamprey (Petromyzon marinus), a fish species with external fertilization that spawns in North Atlantic rivers. Using in vitro fertilization, we made all possible crosses among 10 males and 5 females collected in the spawning grounds. Male identity did not have any significant effect on hatching success. However, female identity and male×female interactions had a highly significant effect on hatching success. Our results suggest that genetic compatibility between male and female genomes plays an important role in embryo survival during the early stages of development in the sea lamprey.
genome interactions; inviability; non-additive genetic variance; external fertilization
The concept of ‘evolvability’ is increasingly coming to dominate considerations of evolutionary change. There are, however, a number of different interpretations that have been put on the idea of evolvability, differing in the time scales over which the concept is applied. For some, evolvability characterizes the potential for future adaptive mutation and evolution. Others use evolvability to capture the nature of genetic variation as it exists in populations, particularly in terms of the genetic covariances between traits. In the latter use of the term, the applicability of the idea of evolvability as a measure of population's capacity to respond to natural selection rests on one, but not the only, view of the way in which we should envisage the process of natural selection. Perhaps the most potentially confusing aspects of the concept of evolvability are seen in the relationship between evolvability and robustness.
evolvability; selection; fitness
Why have some animals evolved large brains despite substantial energetic and developmental costs? A classic answer is that a large brain facilitates the construction of behavioural responses to unusual, novel or complex socioecological challenges. This buffer effect should increase survival rates and favour a longer reproductive life, thereby compensating for the costs of delayed reproduction. Although still limited, evidence in birds and mammals is accumulating that a large brain facilitates the construction of novel and altered behavioural patterns and that this ability helps dealing with new ecological challenges more successfully, supporting the cognitive-buffer interpretation of the evolution of large brains.
brain evolution; cognitive ecology; life history; neurobiology
Demonstrations of interactions between diverse selective forces on bright coloration in defended species are rare. Recent work has suggested that not only do the bright colours of Neotropical poison frogs serve to deter predators, but they also play a role in sexual selection, with females preferring males similar to themselves. These studies report an interaction between the selective forces of mate choice and predation. However, evidence demonstrating phenotypic discrimination by potential predators on these polymorphic species is lacking. The possibility remains that visual (avian) predators possess an inherent avoidance of brightly coloured diurnal anurans and purifying selection against novel phenotypes within populations is due solely to non-random mating. Here, we examine the influence of predation on phenotypic variation in a polymorphic species of poison frog, Dendrobates tinctorius. Using clay models, we demonstrate a purifying role for predator selection, as brightly coloured novel forms are more likely to suffer an attack than both local aposematic and cryptic forms. Additionally, local aposematic forms are attacked, though infrequently, indicating ongoing testing/learning and a lack of innate avoidance. These results demonstrate predator-driven phenotypic purification within populations and suggest colour patterns of poison frogs may truly represent a ‘magic trait’.
aposematic; selection; Dendrobates; magic trait
Infanticide by adult males occurs in a variety of species. While infanticidal attacks have been documented in several equid species in captivity, it has never been witnessed in free-roaming feral horses. I report an infanticide attempt by a free-living feral stallion on a recently born female foal. The stallion picked up the foal by the shoulders, tossed it around twice and bit in on the neck several times. The dam of the foal charged the stallion and successfully protected her foal from additional attacks. The foal survived the attack and later weaned successfully. The stallion recently took over the band and was excluded as the sire through genetic analysis. While this type of attack is rare, this case lends support to the sexual selection hypothesis and further demonstrates that equids have evolved with the risk of infanticide. Furthermore, it shows that maternal protectiveness can be successful against attacks by infanticidal males.
feral horse; maternal protectiveness; sexual selection hypothesis
Many reef fishes change sex during their life. The testing of life-history theory and effective fisheries management therefore relies on our ability to detect when this fundamental transition occurs. This study experimentally illustrates the potential to glean such information from the otolithic bodies of the inner-ear apparatus in the sex-changing fish Parapercis cylindrica. It will now be possible to reconstruct the complete, often complex life history of hermaphroditic individuals from hatching through to terminal reproductive status. The validation of sex-change associated otolith growth also illustrates the potential for sex-specific sensory displacement. It is possible that sex-changing fishes alter otolith composition, and thus sensory-range specificity, to optimize life history in accordance with their new reproductive mode.
reef fish; sex change; otolith; hermaphroditism; life-history transition
The water balance of tsetse flies (Diptera: Glossinidae) has significant implications for understanding biogeography and climate change responses in these African disease vectors. Although moisture is important for tsetse population dynamics, evolutionary responses of Glossina water balance to climate have been relatively poorly explored and earlier studies may have been confounded by several factors. Here, using a physiological and GIS climate database, we investigate potential interspecific relationships between traits of water balance and climate. We do so in conventional and phylogenetically independent approaches for both adults and pupae. Results showed that water loss rates (WLR) were significantly positively related to precipitation in pupae even after phylogenetic adjustment. Adults showed no physiology–climate correlations. Ancestral trait reconstruction suggests that a reduction in WLR and increased size probably evolved from an intermediate ancestral state and may have facilitated survival in xeric environments. The results of this study therefore suggest an important role for water balance physiology of pupae in determining interspecific variation and lend support to conclusions reached by early studies of tsetse physiology.
climate change; geographical range; evolutionary physiology; trypanosomiasis
Theories regarding the role of sexual selection on the evolution of sperm traits are based on an association between pre-copulatory (e.g. female preference) and post-copulatory (e.g. ejaculate quality) male reproductive traits. In tests of these hypotheses, sperm morphology has rarely been used, despite its high heritability and intra-individual consistency. We found evidence of selection for longer sperm through positive phenotypic associations between sperm size and the two major female preference traits in the pied flycatcher, Ficedula hypoleuca. Our results support the sexually selected sperm hypothesis in a species under low sperm competition and demonstrate that natural and pre-copulatory sexual selection forces should not be overlooked in studies of intraspecific sperm morphology evolution.
sperm design; avian reproduction; postcopulatory sexual selection