The evolution and ecology of multiple antipredator defences

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.     

The protective value of the colour and shape of the mountain katydid's antipredator defence

Deimatic behaviour is performed by prey when attacked by predators as part of an antipredator strategy. The behaviour is part of a sequence that consists of several defences, for example they can be preceded by camouflage and followed by a hidden putatively aposematic signal that is only revealed when the deimatic behaviour is performed. When displaying their hidden signal, mountain katydids (Acripeza reticulata) hold their wings vertically, exposing striking red and black stripes with blue spots and oozing an alkaloid-rich chemical defence derived from its Senecio diet. Understanding differences and interactions between deimatism and aposematism has proven problematic, so in this study we isolated the putative aposematic signal of the mountain katydid's antipredator strategy to measure its survival value in the absence of their deimatic behaviour. We manipulated two aspects of the mountain katydid's signal, colour pattern and whole body shape during display. We deployed five kinds of clay models, one negative control and four katydid-like treatments, in 15 grids across part of the mountain katydid's distribution to test the hypothesis that their hidden signal is aposematic. If this hypothesis holds true, we expected that the models, which most closely resembled real katydids would be attacked the least. Instead, we found that models that most closely resembled real katydids were the most likely to be attacked. We suggest several ideas to explain these results, including that the deimatic phase of the katydid's display, the change from a camouflaged state to exposing its hidden signal, may have important protective value.     

Male mate choice in the chameleon grasshopper (Kosciuscola tristis)

In many species, males can increase their fitness by mating with the highest quality females. Female quality can be indicated by cues, such as body size, age and mating status. In the alpine grasshopper Kosciuscola tristis, males can be found riding on subadult females early in the season, and as the season progresses, males engage in fights over ovipositing females. These observations suggest that males may be competing for females that are either unmated (early season) or sperm‐depleted (late season). We thus hypothesised that male K. tristis may be choosy in relation to female mating status, and specifically, we predicted that males prefer females that are unmated. We conducted behavioural experiments in which males were given the choice of two females, one mated and one unmated. Contrary to our prediction, males did not mate preferentially with unmated females. However, copulation duration with unmated females was, on average, 24 times the length of copulation with mated females. While female K. tristis can reject mates, we did not observe any evidence of overt female choice during our trials. Females may gain additional benefits from mating multiply and may therefore not readily reject males. While our experiment cannot definitively disentangle female from male control over copulation duration, we suggest that males choose to invest more time in copula with unmated females, perhaps for paternity assurance, and that male mate assessment occurs during copulation rather than beforehand.     

Similarities in Restriction Fragment Patterns of Mitochondrial DNAs of PhytophthoraSpecies Strongly Depend on the Restriction Enzyme Used Due to Heterogeneous Base Distribution and Sequence Conservation

Mitochondrial DNAs of six morphologically different Phytophthora species were digested with 15 restriction enzymes. The numbers of restriction fragments obtained differed considerably from those theoretically expected for random base distribution. Enzymes with relatively many G and C in their recognition sequences produced significantly larger numbers of fragments. Moreover, fragments generated by most of these enzymes were more often shared by two or more species than those from enzymes with more A and T in their recognition sequence. It is concluded that base distribution in mitochondrial DNA of Phytophthora is heterogeneous,AT-rich stretches occurring scattered over the mitochondrial genome and GC-rich regions present in conserved sequences, presumably genes. A practical consequence for taxonomic RFLP studies is that optimal enzymes can be selected, depending on the desired level of resolution.     

Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences and a review of the evidence for amniote relationships [published erratum appears in Mol Biol Evol 1991 May;8(3):398]

The 18S ribosomal RNAs of 21 tetrapods were sequenced and aligned with five published tetrapod sequences. When the coelacanth was used as an outgroup, Lissamphibia (living amphibians) and Amniota (amniotes) were found to be statistically significant monophyletic groups. Although little resolution was obtained among the lissamphibian taxa, the amniote sequences support a sister-group relationship between birds and mammals. Portions of the 28S ribosomal RNA (rRNA) molecule in 11 tetrapods also were sequenced, although the phylogenetic results were inconclusive. In contrast to previous studies, deletion or down- weighting of base-paired sites were found to have little effect on phylogenetic relationships. Molecular evidence for amniote relationships is reviewed, showing that three genes (beta-hemoglobin, myoglobin, and 18S rRNA) unambiguously support a bird-mammal relationship, compared with one gene (histone H2B) that favors a bird- crocodilian clade. Separate analyses of four other genes (alpha- crystallin A, alpha-hemoglobin, insulin, and 28S rRNA) and a combined analysis of all sequence data are inconclusive, in that different groups are defined in different analyses and none are strongly supported. It is suggested that until sequences become available from a broader array of taxa, the molecular evidence is best evaluated at the level of individual genes, with emphasis placed on those studies with the greatest number of taxa and sites. When this is done, a bird-mammal relationship is most strongly supported. When regarded in combination with the morphological evidence for this association, it must be considered at least as plausible as a bird-crocodilian relationship.      

Prevalence and Molecular Identification of Nematode and Dipteran Parasites in an Australian Alpine Grasshopper (Kosciuscola tristis)

In alpine Australia, Orthoptera are abundant, dominant herbivores, important prey species, and hosts for parasites and parasitoids. Despite the central role of orthopterans in alpine ecosystems, the impact of parasites on orthopteran populations is under-explored. In this study we describe the relationship between parasite prevalence and host sex, body size and year of collection. We accessed an existing, preserved collection of 640 Kosciuscola tristis collected from across its range between 2007 and 2011. Upon dissection we collected juvenile parasites and used molecular tools to identify them to three families (Nematoda; Mermithidae, and Arthropoda: Diptera: Tachinidae and Sarcophagidae). The prevalence of nematodes ranged from 3.5% to 25.0% and dipterans from 2.4% to 20.0%. Contrary to predictions, we found no associations between parasite prevalence and grasshopper sex or size. Although there was an association between prevalence of both nematodes and dipterans with year of collection, this is likely driven by a small sample size in the first year. Our results provide a foundation for future studies into parasite prevalence within the alpine environment and the abiotic factors that might influence these associations.     

Mate guarding and male mate choice in the chameleon grasshopper <Emphasis Type="Italic">Kosciuscola tristis</Emphasis> (Orthoptera: Acrididae)

In the wild, male chameleon grasshoppers (Kosciuscola tristis) are frequently observed mounted on the back of females even when not in copula, and will fight off other usurping males. If this behaviour is mate guarding and reflects investment in male mate choice, then we expect males to preferably guard females based on reliable cues of quality. Cues for female quality likely include female size and egg development that together may indicate fecundity. We investigated male mate choice in the field expressed as mate-guarding preference, by comparing size and egg development in guarded and unguarded females. We found no difference between guarded and unguarded females in measures of fecundity or body size. The majority of females sampled did not contain any viable eggs. This finding suggests that male K. tristis indiscriminately guard females in a scramble mating system.     

Dietary carotenoids change the colour of Southern corroboree frogs

Animal coloration can be the result of many interconnected elements, including the production of colour‐producing molecules de novo, as well as the acquisition of pigments from the diet. When acquired through the diet, carotenoids (a common class of pigments) can influence yellow, orange, and red coloration and enhanced levels of carotenoids can result in brighter coloration and/or changes in hue or saturation. We tested the hypothesis that dietary carotenoid supplementation changes the striking black and yellow coloration of the southern corroboree frog (Pseudophryne corroboree, Amphibia: Anura). Our dietary treatment showed no measurable difference in colour or brightness for black patches in frogs. However, the reflectance of yellow patches of frogs raised on a diet rich in carotenoids was more saturated (higher chroma) and long‐wave shifted in hue (more orange) compared to that of frogs raised without carotenoids. Interestingly, frogs with carotenoid‐poor diets still developed their characteristic yellow and black coloration, suggesting that their yellow colour patches are a product of pteridines manufactured de novo.