Glacial-driven vicariance in the amphipod Gammarus duebeni

We have examined the genetic diversity using mitochondrial COI and ND2 sequence data from 306 specimens of the amphi-Atlantic-distributed amphipod Gammarus duebeni. Marine populations from the Atlantic Ocean, the Baltic and North Sea, as well as freshwater populations from Ireland, Cornwall and Brittany were analysed.G. duebeni is a complex of five allopatric lineages. Freshwater populations result from multiple invasions of marine ancestors, represented by distinct lineages. We interpret the recent distribution of lineages as the outcome of a series of spatio-temporal vicariant events caused by Pleistocene glaciations and sea level changes. The freshwater lineages are therefore regarded as ‘glacial relicts’. Furthermore, inter-specific competition with, for example, Gammarus pulex (which is absent in Ireland and western Brittany) may be another important determinant in the distribution of freshwater G. duebeni. In Ireland and Brittany, three freshwater refugia are suggested. The significantly limited gene flow detected among marine populations is more likely due to inter-specific competition than to salinity. The G. duebeni-complex represents a model system for the study of allopatric speciation accompanied by major habitat shifts. The pattern of spatio-temporal origins of the freshwater entities we describe here provides an excellent system for investigating evolutionary adaptations to the freshwater environment. Our data did not confirm the presently used subspecies classification but are only preliminary in the absence of nuclear genetic analyses.     

Is intersexuality a cost of environmental sex determination in Gammarus duebeni?

Three possible causes of intersexuality in Gammarus duebeni , a crustacean with environmental sex determination, were investigated. Intersexuality appears to be a cost of the flexible sex-determining mechanism of this species: the occurrence of intersexes is influenced by photoperiod, which also cues sex determination. Intersexuality is heritable: intersex mothers produce more intersex offspring than do true females. Parasitism by a feminizing microsporidian is ruled out as a significant cause of intersexuality.     

The breeding behaviour of Gammarus duebeni

The breeding behaviour of a population of Gammarus duebeni is investigated. The breeding system includes a precopulatory guarding phase by a male of a female and the length of this phase varies markedly over the season. Large size is not of as great advantage in reproductive competition between males as in a stream population of G. pulex. In the spring of 1981 oligochete worms, Nais elinguis, were found in the brood pouches of some females; eggs were seldom present with the worms but rather amorphous debris. The occurrence of the worms and the debris in the females' pouches coincided with the pattern of abundance of the worms previously reported.     

Parental control of sex ratio in Gammarus duebeni,an organism with environmental sex determination

Parental sex ratio control was investigated in Gammarus duebeni, an amphipod with an environmentally mediated sex determining system. The effect on the F2 generation sex ratio of the photoperiodic conditions experienced by a) the P generation during and after copulation, b) the F1 generation before and after sex determination, and c) the F2 generation themselves during the period of sex determination, was tested. The photoperiodic conditions the F2 generation experienced during the period of sex determination had a significant effect on their sex ratio (more males were produced under long-day than under short-day conditions), but the photoperiodic conditions experienced by the F1 generation males and females or the P generation on the F1 male's side had no effect on the F2 sex ratio. However, the photoperiodic conditions the P generation on the F1 female's side experienced significantly affected the F2 sex ratio. When these animals experienced long-day conditions the F2 generation became female biased and when they experienced short-day conditions, male biased. It is proposed that the mechanism of control operates through the F1 generation mothers whilst in an embryonic stage of development in the P generation mother's brood pouch. The photoperiodically mediated effects of the embryonic F1 generation mother and the F2 generation on sex determination are additive. A mechanism by which both F1 generation maternal and F2 generation sex ratio control could operate in the field is proposed.     

Adaptive variation in sex determination in a crustacean, Gammarus duebeni

In some animals sex is determined after conception by environmental factors (environmental sex determination. ESD). In the amphipod Gammarus duebeni sex is reportedly determined by photoperiod: there is a higher proportion of males in broods reared under long-day than under short-day photoperiods. It has been proposed that this is an adaptive response to seasonal population dynamics. A test of the hypothesis would be to demonstrate changes in the degree to which sex is determined by the environment in populations from different latitudes with different dynamics. This study reports such a test. Environmental response is significantly less strong in a southern population with a long breeding season than in a northern one in which breeding is seasonally restricted. Moreover, the threshold of the ESD cue for male or female determination is not defined when the breeding season is weakly seasonal. There is a broad correlation between latitude (and hence breeding seasonality) and the strength of ESD response across a series of population studies. Similarities between the Gammarus system of sex determination and that of the Atlantic silverside Menidia menidia, a fish with thermal ESD, are discussed.     

An examination of subspecific differences in the merus of the fifth walking leg of the amphipod Gammarus duebeni Lilljeborg

Stock SL Pinkster (1970) erected two subspecies of Gammarus duebeni primarily on the basis of a difference in the relative dimensions of the merus on the fifth walking leg. The diagnostic feature was given as the ratio of merus length/width, with ratio < 2 in G. duebeni duebeni and ratio > 2 in G. duebeni celticus. It is shown here that the ratio varies with the size of the animal, and this particular ratio is therefore not valid as a taxonomic character. Regressions of log merus width on log merus length were made on large samples of G. duebeni assumed to belong to subspecies celticus and duebeni respectively. The regressions were significantly diiferent and were used to predict that the ratio log merus width/log merus length is relatively constant in both subspecies. Diagnostic values for this ratio were 0.71–0.73 in celticus and 0.74–0.77 in duebeni. The ratio was also determined in small samples of G. duebeni from other localities in western Britain. The morphological difference which characterizes celticus and duebeni was not associated with habitat salinity or with previously determined physiological characteristics. It may be an instance of cHnal variation reinforced by geographical isolation. Regressions of merus length against cephalic length suggest that the relative growth rates of the merus may also differ in the two subspecies.     

Mechanisms of parasite-induced sex reversal in Gammarus duebeni

The amphipod Gammarus duebeni is host to the feminising microsporidian parasite Nosema granulosis that converts males into functional females. To test the hypothesis that the parasite acts through endocrine disruption we compared the morphology of the gonad and activity of the androgenic gland, which coordinates male sexual differentiation, in infected and uninfected animals. Male gonad consisted of testis, seminal vesicle and vas deferens that was anchored to the genital papilla on segment 7. The androgenic gland was associated with the distal end of the vas deferens. In female and intersex animals the bi-lobed ovary opened into the oviduct at segment 5, vestigial vas deferens and vestigial androgenic gland were retained. The majority of parasitised individuals (38/39) were either phenotypic females or intersexes with fully developed ovaries and an undifferentiated androgenic gland. Our data suggest that the parasite prevents differentiation of the androgenic gland. In further support of this hypothesis, mass spectrometry of a single androgenic gland from males revealed a dominant molecular ion with a mass/charge ratio of 4818.4+H, corresponding to a peptide of androgenic gland hormone from Armadillidium vulgare. In contrast the vestigial androgenic gland from parasitised and unparasitised females showed only low intensity peaks. Our observations demonstrate that the parasite manipulates host sex by preventing androgenic gland differentiation, androgenic gland hormone production and consequently male differentiation. This is in agreement with observations of A. vulgare with inherited Wolbachia infection, suggesting that phylogenetically distant feminisers manipulate hosts through a common mechanism. The high frequency of infection in intersexes (89.3%) suggests that this phenotype results from incomplete feminisation by the parasite.     

Morphology and ultrastructure of the organ of Bellonci in the marine amphipod Gammarus setosus

The three-dimensional structure of the organ of Bellonci in the marine amphipod Gammarus setosus and the relationship between its sensory cells and concretion are described using light, transmission, and scanning electron microscopy, with chemical treatment for cell lysis, calcium chelation, glycogen staining, and lanthanum labelling. The organ is encapsulated and has three units called fuselli. Each is enclosed by two fusellar cells which generate and release calcium granule strands into the cores of the fusellar concretions, which are united in the center of the organ. The surface of each fusellus is traversed by spiral dendrites entering dorsally and ending ventrally. The spiral dendrites arise from sensory neurons contained in a palm-shaped ganglion in the center of the capsule, beyond which they are twisted like a rope before reaching the concretion. The spiral dendrites are linked in pairs by gap and tight junctions and each gives origin to two pairs of 9+0 sensory cilia 30 μm apart. The ciliary distal segments give rise to long tubules which are in contact with the calcium granule strands. The ciliary proximal segments are expanded by many long mitochondria which interdigitate with the branched striated ciliary rootlets. The concretion is suspended in the capsule cavity by axons originating from four neurons of a remote mechanoreceptor. The structure of the organ suggests that it is a sensory organ involved in the reception and integration of a variety of stimuli.     

Intersexuality in the amphipod Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis

We investigated the effects of parasitism and temperature on the production of intersexes in the amphipod Gammarus duebeni from a field population at Cumbrae, Scotland. There was significant temporal variation in intersex frequency which ranged from 0.5 to 5.2% in monthly field collections. Prevalence of Nosema granulosis, a feminising microsporidian parasite, also varied temporally and there was a significant correlation between parasite prevalence and intersex frequency in the field. Intersexes (16.3 ± 0.4 mg) were larger than true females (14.8 ± 0.1 mg) but produced fewer eggs thus demonstrating a cost of intersexuality. Intersexes were less likely to be paired than true females. In a breeding experiment, only females infected by N. granulosis produced intersex offspring. Temperature had no effect on intersex frequency. Intersexes therefore appear to be the result of incomplete feminisation by N. granulosis in this population. These results contrast with previous studies of G. duebeni from different populations which found that intersexes were the result of abnormal development under environmental sex determination. We suggest that intersexuality may be induced by both environmental and parasitic factors in populations of G. duebeni. This revised version was published online in August 2006 with corrections to the Cover Date.     

Anaerobic capacity of a crustacean sensitive to low environmental oxygen tensions,the freshwater amphipod Gammarus pulex (L.)

We investigated the accumulation of haemolymph L-lactate in response to anoxia, progressive hypoxia and activity, in a species that rarely encounters low PO₂ in its natural environment, the freshwater amphipod Gammarus pulex (L.). Individuals survived <1.5 h anoxia and accumulated L-lactate in the haemolymph at a rate of 10.26 mmol l^–1 h^–1. No lactate was excreted into the medium during this time. Despite the fact that most individuals of G. pulex were oxyconformers, exposure to acutely declining PO₂s did not result in a switch to anaerobic pathways until PO₂ < 4.4 kPa. Even then the concentrations accumulated remained very low until PO₂ < 0.46 kPa. There was no accumulation of L-lactate in the haemolymph as a result of exhaustive activity. Consequently, it was suggested that (a) it cannot be automatically assumed that anaerobic metabolism is switched on only at the point at which oxyregulation breaks down, (b) that the poor anaerobic capacity observed plays little, if any, role in the metabolic response to hypoxia by Gammarus pulex.     

Geographical,environmental and intrinsic biotic controls on Phanerozoic marine diversification

Abstract: The Paleobiology Database now includes enough data on fossil collections to produce useful time series of geographical and environmental variables in addition to a robust global Phanerozoic marine diversity curve. The curve is produced by a new ‘shareholder quorum’ method of sampling standardization that removes biases but avoids overcompensating for them by imposing entirely uniform data quotas. It involves drawing fossil collections until the taxa that have been sampled at least once (the ‘shareholders’) have a summed total of frequencies (i.e. coverage) that meets a target (the ‘quorum’). Coverage of each interval’s entire data set is estimated prior to subsampling using a variant of a standard index, Good’s u. This variant employs counts of occurrences of taxa described in only one publication instead of taxa found in only one collection. Each taxon’s frequency within an interval is multiplied by the interval’s index value, which limits the maximum possible sampling level and thereby creates the need for subsampling. Analyses focus on a global diversity curve and curves for northern, southern and ‘tropical’ (30°N to 30°S) palaeolatitudinal belts. Tropical genus richness is remarkably static, so most large shifts in the curve reflect trends at higher latitudes. Changes in diversity are analysed as a function of standing diversity; the number, spacing and palaeolatitudinal position of sampled geographical cells; the mean onshore–offshore position of cells; and proportions of cells from carbonate, onshore and reefal environments. Redundancy among the variables is eliminated by performing a principal components analysis of each data set and using the axis scores in multiple regressions. The key factors are standing diversity and the dominance of onshore environments such as reefs. These factors combine to produce logistic growth patterns with slowly changing equilibrium values. There is no evidence of unregulated exponential growth across any long stretch of the Phanerozoic, and in particular there was no large Cenozoic radiation beyond the Eocene. The end‐Ordovician, Permo–Triassic and Cretaceous–Palaeogene mass extinctions had relatively short‐term albeit severe effects. However, reef collapse was involved in these events and also may have caused large, longer term global diversity decreases in the mid‐Devonian and across the Triassic/Jurassic boundary. Conversely, the expansion of reef ecosystems may explain newly recognized major radiations in the mid‐Permian and mid‐Jurassic. Reef ecosystems are particularly vulnerable to current environmental disturbances such as ocean acidification, and their decimation might prolong the recovery from today’s mass extinction by millions or even tens of millions of years.     

Condition-dependent ecdysis and immunocompetence in the amphipod crustacean,Gammarus pulex

The exoskeleton of arthropods forms an efficient protection against pathogens, but this first line of defence is periodically weakened during ecdysis, increasing the opportunity for surrounding pathogens to invade the body cavity. Since the richness of pathogens in the environment can be spatially and temporally variable, arthropods may have a fitness advantage in moulting in a place and time of low infection risk. Consistent with this hypothesis, we found that the amphipod crustacean, Gammarus pulex, exhibits temporal adjustment of the moult cycle in response to elevated risks of infection. Interestingly, this phenomenon is variable between two populations and independent of levels of immune defences. These results suggest that plasticity of the moult cycle in response to elevated risks of infection is adaptive and may result from adaptation to local variations in the risk of infection.     

Precopulatory mate guarding in an amphipod,Gammarus lawrencianus bousfield

Traditional theoretical accounts of crustacean mate guarding have assumed that changes associated with the female's reproductive state elicit the mate guarding behaviour of the male. The present study systematically examined the effects of both the male and female reproductive states on the precopulatory mate guarding decision of the amphipod Gammarus lawrencianus. Independent manipulation of the male and female variables indicated that both contributed additively to the probability of precopulatory mate guarding. When considered together, the results demonstrate that females that are closer to the post-moult copulation state are more likely to be guarded; and that males are more likely to enter the mate guarding relationship as the time since their last copulation increases. An adequate theoretical account of crustancean precopulatory mate guarding must, therefore, consider the contribution of both the male and the female reproductive states to the mate guarding decision.     

Effects of oil on the amphipod Gammarus oceanicus

The effects of a number of oils (one crude and two refined products) were tested under various conditions on larvae and adults of the amphipod Gammarus oceanicus. Acute toxicity tests were performed, as well as long-term bioassays. Larvae were found to be several hundred times more sensitive to the oils than the adults during acute exposure. A number of sublethal effects appeared during long-term bioassays. The adults showed impaired swimming performance, decreased tendency to precopulate, impaired light reaction and decreased production of larvae. Decreased growth was found among larvae during chronic exposure to crude oil. Delayed mortality occurred among adults after a short-term exposure to crude oil with a long recovery period.     

Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni

The amphipod crustacean Gammarus duebeni hosts two species of vertically transmitted microsporidian parasites, Nosema granulosis and Microsporidium sp. A. Here it is demonstrated that these co-occurring parasite species both cause infected females to produce female-biased broods. A survey of European G. duebeni populations demonstrates that these two parasites co-occur in six of 10 populations. These findings contrast with the theoretical prediction that two vertically transmitted feminizing parasites should not coexist in a panmictic population of susceptible hosts at equilibrium. Possible explanations for the co-occurrence of the two feminizing microsporidia in G. duebeni include the recent invasion of a new parasite, horizontal transmission of one or both parasites and the spread of alleles for resistance to the dominant parasite in host populations.     

Life-history and production of the amphipod Gammarus pulex in a Dorset chalk stream

SUMMARY. The seasonal variation in population density of Gammarus pulex was studied in a Dorset chalk stream. The numbers increased markedly in June and July and reached a maximum of c. 10000m⁻² in September whilst the most rapid decline in density occurred in October-November and reached a minimum of 820 m⁻² in February. The animals occurred in greater densities in habitats containing Ranunculus or Callitriche than in those devoid of vegetation. The population structure was determined monthly and was split into juveniles (length <4mm), immature males, immature females, mature males and ovigerous females. The percentage of juveniles (39–76) was always the highest of any of the categories. Ovigerous females were found at all times of the year. The sex ratio varied with the time of year both for immatures and matures, although there was approximately a 1:1 ratio for the mature individuals. Seasonal variation in biomass showed a maximum of 7.l g dry wt m⁻² in September and a minimum of 1.4 g dry wt m⁻² in March. Production was calculated by two methods giving values of 12.9 g dry wt m⁻² year⁻¹ and 12.8 g dry wt m⁻² year⁻¹.