School of Biological Sciences
A general mechanism for conditional expression of sexually-selected traits
Author(s): Warren, IA
Exaggerated sexually-selected traits are widespread across nature, with the “classic” examples including the trains of peacocks and antlers of cervids. These traits have provided the focus of many models and much debate concerning how they have evolved and how they are maintained. It is clear that these traits are reliable signals of the bearer’s condition, but the underlying physiological mechanism required to achieve such exaggerated and highly condition dependent growth has remained, until recently, unclear. Handicap models have been proposed but lack consistent experimental support. Using the horned rhinoceros beetle, Trypoxylus dichotomus, we demonstrate that the insulin-like signaling (ILS) pathway can provide a robust and reliable physiological mechanism for generating an informative signal of individual condition. The ILS pathway is a highly conserved pathway that can regulate growth in response to nutritional level, stress and infection. Exaggerated and highly condition dependent growth in beetle horns is achieved by heightened sensitivity of the developing horn primorida to the ILS pathway, when compared to other traits such as wings and genitalia. This result, combined with evidence from a wide range of taxa (e.g. crustaceans, cervids and fish), as well as the highly conserved nature of the ILS pathway, raises the exciting possibility that parallel processes underlie the evolution of trait exaggeration in a multitude of sexually-selected signal traits across the animal kingdom.
A novel approach to study phenotypic evolution in an adaptive radiation: x-ray images provide novel insights into the adaptive radiation of cichlid fishes in East African Lake Tanganyika
Author(s): Colombo, M, Meury, F, Büscher, H, Salzburger, W
The East African Great Lakes, Tanganyika, Victoria and Malawi, are ecosystems with highly diverse habitats and food resources and renowned for the spectacular adaptive radiations of cichlid fishes that they contain. Lake Tanganyika harbors a highly diverse cichlid species flock comprising more than 220 species that are morphologically and ecologically highly diverse, but also show a number of convergent cichlid species that have evolved within the lake. Here, we use a novel approach to study convergence and divergence in Lake Tanganyika cichlids, making use of about 5000 x-ray images of more than 160 Tanganyikan cichlid species. We used geometric morphometric as well as meristic measurements in combination with ecological data (stable-isotopes) and a molecular phylogeny to examine the patterns of diversification in a large cichlid radiation. Furthermore, we were interested in testing predictions regarding adaptive radiation, such as its progress in stages, the early-burst scenario and the correlation between phenotypes and the environment. We identified various instances of convergent evolution within the adaptive radiation of cichlid fishes in Lake Tanganyika, particularly regarding body elongation and benthic or pelagic lifestyles and show a relatively constant rate in phenotypic evolution. Our study thus deepens the understanding of how cichlids diversify and how morphologies changed as species adapted to different habitats and foraging modes.
Department of Biology
A resampling-based approach to study variation in morphological modularity
Author(s): Fruciano, C, Franchini, P, Meyer, A
Modularity has been suggested to be connected to evolvability because an higher degree of independence among parts allows them to evolve as separate units. Recently, the Escoufier RV coefficient has been proposed as a measure of morphological modularity in multivariate morphometric datasets. However, it has been shown, using randomly simulated datasets, that the value of the RV coefficient depends on sample size. Also, so far there is no statistical test for the difference in modularity between a priori defined groups. Here we: 1. using a rarefaction analysis, show that the value of the RV Escoufier coefficient depends on sample size also in real morphometric datasets; 2. propose a permutation procedure to test for the difference in the RV coefficient between a priori defined groups; 3. show, through simulations, that such a permutation procedure has an appropriate Type I error. The permutation procedure outlined here, readily extendable to non-morphometric datasets, will allow statistically sound comparisons of the degree of modularity between a priori defined groups.
Alteration of HPA/HPG axis reactivity as a consequence of chicken domestication
Author(s): Fallahshahroudi, A, Ericsson, M, Bergquist, J, Kushnir, MM, Jensen, P
Domesticated animals can serve as models to study evolutionary processes. The hormonal stress responses of wild and domesticated animals have rarely been thoroughly compared. The Red Jungle fowl (RJF) is considered to be the main ancestor of all domesticated chicken breeds. The aim of this study was to investigate the impact of domestication on behaviour and reactivity of HPA/HPG axis to a stressful physical restraint episode. Using liquid chromatography tandem mass spectrometry methods (LC-MS/MS), plasma concentrations of 5 classes of steroids, namely, pregnanes, progestines, androgens, estrogens and glucocorticoids were measured at basal level, 10 and 60 minutes after restraint in domesticated female White Leghorn (WL) and RJF. In behaviour tests, WL had a slower stress recovery, whilst RJF resumed baselines in behaviour more quickly. Corticosterone level was significantly influenced by the stressor (p ≤ 0.001) in both breeds. RJF had significantly higher acute stress response (p ≤0.05) but quicker stress recovery compared to WL. In RJF, most other hormones were not influenced by the stressor while they were mostly significantly affected in the domesticated WL. Among the hormones which were differently altered in WL and RJF, dehydroepiandrosterone (DHEA), an androgen which is also involved in social and aggressive behaviour in birds, showed the most pronounced breed difference (p ≤ 0.005) and response to stress (p ≤ 0.001) in WL and might be highlighted as an important hormone in relation to both stress and domestication of chicken. To our knowledge this is the first comprehensive study, investigating the impact of stress on behaviour and a wide range of steroid and neurosteroid hormones in any domesticated animal and it´s wild ancestor. In conclusion, our study shows that the domesticated phenotype in chicken is related to lower HPA axis reactivity and higher HPG axis activity, which cannot be maintained in stressful situations.
Laboratoire d'Excellence CORAIL
Anthropogenic disturbances on the development and physiology of marine species
Author(s): Mills, SC, Beldade, R, Bernardi, G, Bigot, L, Chabanet, P, Holles, S, Mourrier, J, O'Donnell, J, Planes, S, Radford, A, Simpson, S
Natural and human-induced disturbances across aquatic and terrestrial habitats affect a broad range of species and communities causing declines in both biodiversity and population abundance. Whilst habitat disturbances are known to affect species’ distributions, phenology and physiology, less is known about the effects on development and stress physiology, especially for marine species. We investigated how a range of disturbances, mainly anthropogenic, affected the development and stress physiology of different tropical marine species. We will describe how two different habitat disturbances, the 1998 global bleaching event that reduced live coral cover and chronic boat noise, increased levels of the teleost stress hormone, cortisol in the skunk anemonefish and three-spot damselfish respectively. We will also describe how shark- and ray-feeding dive sites interact with insulin and gonadal steroid hormones of the black-tipped reef shark. Finally, we will describe how chronic boat noise slows sea hare embryonic development and reduces veliger hatching success. We will discuss how these varying habitat disturbances could impact reproduction and survival, highlighting their consequences for population dynamics.
Department of Systematic Zoology and Ecology
Behavioural consistency in Rana temporaria tadpoles: strong personalities, lack of syndromes and link to life-history
Author(s): Herczeg, G, Urszán, TJ, Hettyey, A, Török, J
Recent interest in evolutionary behavioural ecology has turned towards understanding the causes and consequences of behavioural consistency, manifesting either as animal personality (i.e. consistency in a single behaviour) or behavioural syndromes (i.e. consistency across two or more behaviours). Further, behavioural consistency has been linked to life-history strategies currently, possibly forming integrative pace-of-life syndromes (POLS). However, empirical tests of this theory are extremely scarce. Here, we tested, using agile frog (Rana dalmatina) tadpoles as model, if POLS could be detected in the larval stage of amphibians based on a common garden experiment targeting two ontogenetic stages and measuring three behavioural traits. Activity was consistent in the early stage and was negatively related to age at metamorphosis. In the later stage, activity, exploration and risk-taking was all consistent, but their relationship with life-history depended on whether the studied individuals were tested in the earlier stage or not. Already tested individuals showed no POLS, but both activity (negatively) and risk-taking (positively) was related to age at metamorphosis in their previously untested conspecifics. We only detected one behavioural syndrome: activity and risk-taking was strongly negatively correlated in the previously tested (i.e. disturbed) group. Our results provide evidence for (i) animal personality in tadpoles, (ii) an activity – metamorphosis-timing POLS and (iii) an unexpectedly strong effect of moderate disturbance related to standard behavioural testing on later behavioural consistency.
Department of Ecology & Genetics
Brain size and personality: artificial selection reveals a positive genetic correlation between brain size and proactivity in the guppy
Author(s): Lievens, EJP, Kotrschal, A, Dahlbom, J, Bundsen, A, Semenova, S, Sundvik, M, Maklakov, AA, Winberg, S, Panula, P, Kolm, N
Animal personalities range from shy, cautious, easily stressed individuals (‘reactive’ personality types) to bold, innovative individuals that are prone to risk-taking and routine formation (‘proactive’ personality types). Though personality differences are expected to have important fitness consequences, their underlying mechanisms remain enigmatic. In this study, we investigated the relationship between individual differences in personality and variation in brain size. We performed three standard personality assays using populations of guppies (Poecilia reticulata) under artificial selection for large and small relative brain size, which also have known differences in cognitive ability. First, large-brained guppies were faster to habituate and more exploratory when tested in an open field; large-brained females were also bolder. Second, large-brained animals excreted less cortisol in a stressful confinement test. Finally, large-brained individuals were slower to adopt a novel food source, a result which is likely due to stronger routine formation rather than lack of innovation. Overall, our findings indicate that large-brained animals have a more proactive personality type, a characteristic which may affect important aspects of their ecology such as dispersal and niche exploration.
Institute of Environmental Sciences
Characterization of sex-biased genes from the transcriptome of a male-dimorphic mite
Author(s): Stuglik, MT, Babik, W, Radwan, J
The different sexes experience different selective pressures, which can lead to highly divergent phenotypes that are achieved via sex-biased gene expression. As a result of sexual selection and sexual conflict, sex-biased genes are expected to evolve at a faster rate than other genes in the genome. Furthermore, because sexual selection acts more strongly on males, male-biased genes are expected to evolve faster than female-biased genes. We aimed to test these predictions in a model species for sexual selection and conflict research, the bulb mite Rhizoglyphus robini (Acari, Acaridae), in which armored, aggressive fighter males coexist with unarmored scrambler males. We sequenced and de-novo assembled transcriptomes of adult males and females. Expression of 4.0% of 114,456 transcriptome-based gene models (TGMs) was male-biased, whereas 1.3% of TGMs had female-biased expression and this difference was highly significant. For TGMs with protein-coding capacity, the proportion with orthologs identified in the spider mite (Tetranychus urticae) genome was lower for male-biased than for unbiased genes, but was very similar for female-biased and unbiased genes. Mean amino acid distances between male-biased R. robini genes and their T. urticae orthologs were significantly greater than those between unbiased genes and their orthologs; female-biased gene orthologs had distances similar to those of the unbiased orthologs. The higher number and faster evolution of male-biased genes are consistent with the hypothesis that sexual dimorphism is driven mostly by male-biased sexual selection. This hypothesis is further supported by the result that the fighter morph, which is behaviorally and morphologically adapted to intense intrasexual competition, was characterized by a considerably larger number of overexpressed (compared to female expression levels) genes than the less sexually dimorphic scrambler morph.
Department of Zoology
Co-option of host-alternating polyphenism in the evolution of caste polyphenism in social aphids
Author(s): Uematsu, K, Shibao, H
Castes in social insects are one of the most well-known examples of polyphenism. However, the developmental origins of the discrete alternative phenotypes are largely unknown. Social aphids form galls on their primary host plant and open colonies on their secondary host plant, producing different phenotypes on each plant. Aphids of the genus Colophina form galls on Zelkova trees in spring. Winged aphids migrate from mature galls in summer and then found open colonies on Clematis plants. In the galls, polyphenism does not occur and the aphids produce first-instar defenders that attack predators with mouthparts. In the open colonies, first-instar sterile soldiers with enlarged legs and shortened mouthparts are produced from polyphenic development. The morphology and defensive behaviour of the soldiers in the open colonies resembles those of monomorphic defenders in the galls, suggesting the possibility that these two defensive morphs share a common developmental program. To investigate the genetic relationship between defenders of Zelkova trees and soldiers of Clematis colonies, I compared morphological traits of four Colophina species. Body parts of the following morphs were measured: 1. monomorphic first-instar nymphs of Zelkova galls, 2. reproductive first-instar nymphs of Clematis colonies, 3. soldier first-instar nymphs of Clematis colonies. Morphometric analyses showed a positive correlation between the morphology of the first-instar nymphs in galls and the sterile soldiers in open colonies. Moreover, in the species close to their ancestral condition, both phenotypes were almost identical. These results suggest that the soldier caste of Colophina species first evolved by co-option from ancestral host-alternating polyphenism, and diverged to have specialized morphology. I will also discuss ecological factors favouring the evolution of the sterile castes, and the contribution of inclusive fitness to the evolution of a novel phenotype.
Department of Biology
Conflict and co-adaptation: the evolution of parental care in a wild bird species
Author(s): Lucass, C, Eens, M, Müller, W
Interactions between caring parents and their offspring are one of the most widespread social behaviours in animals. Parent-offspring interactions involve two parties and its evolution is, therefore, dependent on the evolution of two traits, parental provisioning and offspring begging. From a quantitative genetic perspective both behaviours should co-adapt, which should ultimately lead to (genetic) co-variation. This hypothesis is supported by a number of recent empirical studies. However, most of these studies have been performed in captivity under controlled environmental conditions. This limits the information on among others fitness costs, while these costs are thought to stabilize the process of co-adaptation. By means of a cross-fostering experiment, we studied co-adaptation of offspring begging and parental provisioning in free-living blue tits (Cyanistes caeruleus), thus in the presence of natural selection. We did find evidence for co-adaptation, but only in male parents, as the paternal feeding rates co-varied with begging intensities of their genetic chicks, which were raised in foster nests. By contrast, feeding rates of females co-varied with the begging intensity of the foster chicks they were raising. We can think of two hypotheses that may explain the observed pattern: First, the co-variation in males may reflect a (general) genetic correlation between parental feeding rates and offspring begging, which may be masked in females due to a higher responsiveness to offspring need (thus foster chick begging). A higher responsiveness to actual need in females may also indicate that they may compensate for deviations between offspring begging and paternal feeding. Second, the co-variation of fathers’ feeding rate with their genetic offspring’s begging may relate to prenatal maternal effects, with mothers interlinking offspring begging (possibly via differently allocation of egg compounds) to the males’ expected contribution to parental care.