Sperm competition and the evolution of testes size in terrestrial mammalian carnivores

Summary Understanding the factors influencing variation in the degree of sperm competition is a key question underlying the mechanisms driving sexual conflict. Previous behavioural and comparative studies have indicated that carnivores appear to have evolved under sperm competition but an analysis of the predictors of the level of sperm competition is missing. In this study, we use phylogenetic comparative methods to investigate life-history parameters predicted to affect the degree of sperm competition in terrestrial carnivores using variation in relative testes size (RTS, after controlling for body size allometry) as a measure of the level of sperm competition. Due to a paucity of consistent data across taxa, we used three measures of RTS: testes mass (n = 40 species), testes and epididymes mass combined (n = 38), and testes volume (n = 48). We also created a derived data set (n = 79) with testes mass estimated from regression analyses on the other measures of testes size. Carnivores with shorter mating seasons had relatively larger testes, consistent with the hypothesis that sperm competition is greater when the degree of female oestrous synchrony is high. This relationship was stronger in spontaneous versus induced ovulators, suggesting higher sperm competition levels in spontaneous ovulators. This is the first comparative study to show this within mammalian taxa. Neither social mating system nor reproductive lifespan were significantly associated with variation in RTS and hence are poor predictors of sperm competition levels. None of the above relationships were found to be significant for the testes and epididymes mass combined data set, but our understanding of the role of the epididymis in sperm competition is too limited to draw any conclusions. Finally, we consistently found a significant phylogenetic signal in all analyses, indicating that phylogeny has played a significant role in the evolution of carnivore testes size and, therefore, in shaping levels of sperm competition. Our results shed new light into the factors affecting levels of sperm competition in terrestrial carnivores by showing that the degree of oestrous synchrony and ovulation type interact to predict variation in RTS.

Phylogeny, biogeography, and ecology of Ficus section Malvanthera (Moraceae)

We conducted the first molecular phylogenetic study of Ficus section Malvanthera (Moraceae; subgenus Urostigma) based on 32 Malvanthera accessions and seven outgroups representing other sections of Ficus subgenus Urostigma. We used DNA sequences from the nuclear ribosomal internal and external transcribed spacers (ITS and ETS), and the glyceraldehyde-3-phosphate dehydrogenase (G3pdh) region. Phylogenetic analysis using maximum parsimony, maximum likelihood and Bayesian methods recovered a monophyletic section Malvanthera to the exclusion of the rubber fig, Ficus elastica. The results of the phylogenetic analyses do not conform to any previously proposed taxonomic subdivision of the section and characters used for previous classification are homoplasious. Geographic distribution, however, is highly conserved and Melanesian Malvanthera are monophyletic. A new subdivision of section Malvanthera reflecting phylogenetic relationships is presented. Section Malvanthera likely diversified during a period of isolation in Australia and subsequently colonized New Guinea. Two Australian series are consistent with a pattern of dispersal out of rainforest habitat into drier habitats accompanied by a reduction in plant height during the transition from hemi-epiphytic trees to lithophytic trees and shrubs. In contradiction with a previous study of Pleistodontes phylogeny suggesting multiple changes in pollination behaviour, reconstruction of changes in pollination behaviour on Malvanthera, suggests only one or a few gains of active pollination within the section. (C) 2008 Elsevier Inc. All rights reserved.

Identification of trade-offs underlying the primary strategies of plants

Question: What are the key physiological and life-history trade-offs responsible for the evolution of different suites of plant traits (strategies) in different environments? Experimental methods: Common-garden experiments were performed on physiologically realistic model plants, evolved in contrasting environments, in computer simulations. This allowed the identification of the trade-offs that resulted in different suites of traits (strategies). The environments considered were: resource rich, low disturbance (competitive); resource poor, low disturbance (stressed); resource rich, high disturbance (disturbed); and stressed environments containing herbivores (grazed). Results: In disturbed environments, plants increased reproduction at the expense of ability to compete for light and nitrogen. In competitive environments, plants traded off reproductive output and leaf production for vertical growth. In stressed environments, plants traded off vertical growth and reproductive output for nitrogen acquisition, contradicting Grime's (2001) theory that slow-growing, competitively inferior strategies are selected in stressed environments. The contradiction is partly resolved by incorporating herbivores into the stressed environment, which selects for increased investment in defence, at the expense of competitive ability and reproduction. Conclusion: Our explicit modelling of trade-offs produces rigorous testable explanations of observed associations between suites of traits and environments.

Fitness costs of dispersal in red foxes (Vulpes vulpes)

The costs of dispersal are an important factor promoting natal philopatry, thereby encouraging the formation of social groups. The red fox, Vulpes vulpes, exhibits a highly flexible social system and one that is thought to represent a possible stage in the evolution of more complex patterns of group-living. Although the potential benefits accruing to philopatric offspring have previously been studied in this species, the potential costs of dispersal have received less attention. We contrasted survival rates, nutritional status, injuries and reproductive output of dispersing and non-dispersing male and female foxes in an urban population to assess the relative costs of dispersal versus natal philopatry. Mortality rates were not significantly higher for dispersing foxes, either in the short- or long-term. There was no evidence of increased nutritional stress in dispersing individuals. Dispersing individuals did, however, exhibit greater levels of wounding, although this did not appear to affect survival. Dispersing females were more likely to miss a breeding opportunity early in their reproductive lifespan. In contrast, both dispersing and non-dispersing males were unlikely to breed in their first year. We conclude that the major fitness component in females affected by dispersing is age at first reproduction.

Developmental programming: Deficits in reproductive hormone dynamics and ovulatory outcomes in prenatal, testosterone-treated sheep

Prenatal testosterone excess leads to neuroendocrine, ovarian, and metabolic disruptions, culminating in reproductive phenotypes mimicking that of women with polycystic ovary syndrome (PCOS). The objective of this study was to determine the consequences of prenatal testosterone treatment on periovulatory hormonal dynamics and ovulatory outcomes. To generate prenatal testosterone-treated females, pregnant sheep were injected intramuscularly (days 30-90 of gestation, term = 147 days) with 100 mg of testosterone-propionate in cottonseed oil semi-weekly. Female offspring born to untreated control females and prenatal testosterone-treated females were then studied during their first two breeding seasons. Sheep were given two injections of prostaglandin F-2alpha 11 days apart, and blood samples were collected at 2-h intervals for 120 h, 10-min intervals for 8 h during the luteal phase (first breeding season only), and daily for an additional 15 days to characterize changes in reproductive hormonal dynamics. During the first breeding season, prenatal testosterone-treated females manifested disruptions in the timing and magnitude of primary gonadotropin surges, luteal defects, and reduced responsiveness to progesterone negative feedback. Disruptions in the periovulatory sequence of events during the second breeding season included: 1) delayed but increased preovulatory estradiol rise, 2) delayed and severely reduced primary gonadotropin surge in prenatal testosterone-treated females having an LH surge, 3) tendency for an amplified secondary FSH surge and a shift in the relative balance of FSH regulatory proteins, and 4) luteal responses that ranged from normal to anovulatory. These outcomes are likely to be of relevance to developmental origin of infertility disorders and suggest that differences in fetal exposure or fetal susceptibility to testosterone may account for the variability in reproductive phenotypes.

Life-history evolution under a production constraint

The recently formulated metabolic theory of ecology has profound implications for the evolution of life histories. Metabolic rate constrains the scaling of production with body mass, so that larger organisms have lower rates of production on a mass-specific basis than smaller ones. Here, we explore the implications of this constraint for life-history evolution. We show that for a range of very simple life histories, Darwinian fitness is equal to birth rate minus death rate. So, natural selection maximizes birth and production rates and minimizes death rates. This implies that decreased body size will generally be favored because it increases production, so long as mortality is unaffected. Alternatively, increased body size will be favored only if it decreases mortality or enhances reproductive success sufficiently to override the preexisting production constraint. Adaptations that may favor evolution of larger size include niche shifts that decrease mortality by escaping predation or that increase fecundity by exploiting new abundant food sources. These principles can be generalized to better understand the intimate relationship between the genetic currency of evolution and the metabolic currency of ecology.

The use of image analysis to estimate population growth rate in Daphnia magna

1. Population growth rate (PGR) is central to the theory of population ecology and is crucial for projecting population trends in conservation biology, pest management and wildlife harvesting. Furthermore, PGR is increasingly used to assess the effects of stressors. Image analysis that can automatically count and measure photographed individuals offers a potential methodology for estimating PGR. 2. This study evaluated two ways in which the PGR of Daphnia magna, exposed to different stressors, can be estimated using an image analysis system. The first method estimated PGR as the ratio of counts of individuals obtained at two different times, while the second method estimated PGR as the ratio of population sizes at two different times, where size is measured by the sum of the individuals' surface areas, i.e. total population surface area. This method is attractive if surface area is correlated with reproductive value (RV), as it is for D. magna, because of the theoretical result that PGR is the rate at which the population RV increases. 3. The image analysis system proved reliable and reproducible in counting populations of up to 440 individuals in 5 L of water. Image counts correlated well with manual counts but with a systematic underestimate of about 30%. This does not affect accuracy when estimating PGR as the ratio of two counts. Area estimates of PGR correlated well with count estimates, but were systematically higher, possibly reflecting their greater accuracy in the study situation. 4. Analysis of relevant scenarios suggested the correlation between RV and body size will generally be good for organisms in which fecundity correlates with body size. In these circumstances, area estimation of PGR is theoretically better than count estimation. 5. Synthesis and applications. There are both theoretical and practical advantages to area estimation of population growth rate when individuals' reproductive values are consistently well correlated with their surface areas. Because stressors may affect both the number and quality of individuals, area estimation of population growth rate should improve the accuracy of predicting stress impacts at the population level.

Towards a population ecology of stressed environments: the effects of zinc on the springtail Folsomia candida

1. To understand population dynamics in stressed environments it is necessary to join together two classical lines of research. Population responses to environmental stress have been studied at low density in life table response experiments. These show how the population's growth rate (pgr) at low density varies in relation to levels of stress. Population responses to density, on the other hand, are based on examination of the relationship between pgr and population density. 2. The joint effects of stress and density on pgr can be pictured as a contour map in which pgr varies with stress and density in the same way that the height of land above sea level varies with latitude and longitude. Here a microcosm experiment is reported that compared the joint effects of zinc and population density on the pgr of the springtail Folsomia candida (Collembola). 3. Our experiments allowed the plotting of a complete map of the effects of density and a stressor on pgr. Particularly important was the position of the pgr= 0 contour, which suggested that carrying capacity varied little with zinc concentration until toxic levels were reached. 4. This prediction accords well with observations of population abundance in the field. The method also allowed us to demonstrate, simultaneously, hormesis, toxicity, an Allee effect and density dependence. 5. The mechanisms responsible for these phenomena are discussed. As zinc is an essential trace element the initial increase in pgr is probably a consequence of dietary zinc deficiency. The Allee effect may be attributed to productivity of the environment increasing with density at low density. Density dependence is a result of food limitation. 6. Synthesis and applications. We illustrate a novel solution based on mapping a population's growth rate in relation to stress and population density. Our method allows us to demonstrate, simultaneously, hormesis, toxicity, an Allee effect and density dependence in an important ecological indicator species. We hope that the approach followed here will prove to have general applicability enabling predictions of field abundance to be made from estimates of the joint effects of the stressors and density on population growth rate.

Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance

The influence of sedimentation, depth and substratum angle on sponge assemblages in the Wakatobi region, south-eastern Sulawesi, Indonesia was considered. Sponge assemblages were sampled from two reef localities. The first reef (Sampela) was highly impacted by high sedimentation rates with fine sediment particles that settle slowly, while the second (Hoga) experienced only fast settling coarse sediment with lower overall sedimentation rates. Sponge assemblages were sampled (area occupied and numbers) on the reef fiat (0 m) and at 5 (reef crest), 10 and 15 m (15 m at Hoga only). Some significant (P < 0.001) differences were observed in the area occupied and the number of sponge patches between surface angles and sites. Significantly lower (t > 4.61, df = 9, P < 0.001) sponge numbers, percentage cover and richness were associated with the reef flat at both sites compared with all other depths at each site, with the exception of abundance of sponges on the reef flat at Sampela, which was much greater than at any other depth sampled. Species richness increased with depth at both sites but differences between surface angles were only recorded at Sampela, with higher species richness being found on vertical, inclined and horizontal surfaces respectively A total of 100 sponge species (total area sampled 52.5 m(2)) was reported from the two sites, with 58 species found at Sampela and 71 species at Hoga (41% of species shared). Multi-dimensional scaling (MDS) indicated differences in assemblage structure between sites and most depth intervals, but not substratum angles. A number of biological (e.g. competition and predation) and physical (e.g. sedimentation and aerial exposure) factors were considered to control sponge abundance and richness. Unexpectedly a significant (F-1,F-169 = 148.98, P < 0.001) positive linear relationship was found between sponge density and area occupied. In areas of high sponge coverage, the number of patches was also high, possibly due to fragmentation of large sponges produced as a result of predation and physical disturbance. The MDS results were also the same whether sponge numbers or percentage cover estimates were used, suggesting that although these different approaches yield different sorts of information, the same assemblage structure can be identified.

The reproductive response of rams to thyroidectomy: mediation by impaired inhibin feedback rather than a change in LH pulsatility

A series of experiments was conducted to examine the mechanism by which removal of the thyroid glands in seasonally suppressed rams brings about rapid testicular growth. In the first experiment, thyroidectomy at the nadir of the testicular cycle (late winter) initiated testis growth without any detectable change in the extent of spermatogenesis compared with sham-operated controls. The serum concentration of FSH, but not LH, was also markedly increased by thyroidectomy. In the second experiment, serum FSH concentration was again increased by thyroidectomy in late winter but there was no effect of thyroidectomy on LH concentration, LH pulses (measured in frequent blood samples) or testosterone concentration. Furthermore, there was no evidence of a change in central dopaminergic inhibition of GnRH, as measured by the pulsatile LH response to an i.m. injection of the dopaminergic D-2 agonist bromocriptine or antagonist sulpiride. The rapid increase in FSH concentration occurred despite a markedly increased serum inhibin A concentration in thyroidectomized rams. Therefore, the efficacy of inhibin feedback was examined by testing the FSH-suppressive effect of an inhibin preparation (5 ml charcoal-stripped bovine follicular fluid i.v.) in long-term thyroidectomized and thyroid intact castrated rams. Bovine follicular fluid suppressed FSH concentrations in control rams as expected but in marked contrast, was completely without effect in thyroidectomized animals. In castrated rams, the FSH concentration was only marginally increased by thyroidectomy, indicating that there is a major component of the mediation of the effects of thyroidectomy that is testicular in origin. It was concluded that a reduction in the ability of endogenous inhibin to inhibit FSH release at the pituitary, rather than a hypothalamic mechanism, is the primary cause of the stimulation of testis growth by thyroidectomy.

Reproductive biology and population studies in two annual shuttle mosses

Observations on clumps of Phascum cuspidatum during the summer and autumn indicated that this species is at least a short-lived perennial, as young shoots develop from old, brown shoots persisting from the previous winter. No young shoots arising by vegetative propagation were recorded in Pottia truncata. Rhizoid tubers were observed in this species, but only in one of the many clumps examined. Spores of both species germinated freely in culture, but when spores were planted in the field young gametophytes developed inconsistently in P. truncata and never in P. cuspidatum. An investigation of spore deposition around an isolated clump of P. truncata suggested that 67% of the spores released were deposited within the clump, and 70% within 2m. Electrophoretic studies indicated limited genetic variation within two populations of each species, with no genotypes in common between the populations. No genetic variation was recorded between gametophytes within individual clumps of either species, nor between sporophytes and their maternal gametophytes, suggesting a high incidence of inbreeding in these monoecious mosses. (author abst.)