Differences in genetic structure and ecological diversity between parental forms and hybrids in a Daphnia species complex

Hybridization is a common phenomenon in Daphnia species complexes. Hybrids often dominate in Daphnia populations; therefore it is worthwhile to look for principal differences between parental and hybrid populations with respect to their genetic structure and clonal differentiation. We studied natural populations of members of the Daphnia galeata/hyalina/cucullata complex in three lakes. In one of these lakes, one parental species (D. galeata) and one hybrid (D. galeata × cucullata) were investigated more intensively. The frequency of sexual reproduction was higher in parental populations, whereas clonal diversity was higher in hybrid populations. Ecological differentiation among clonal groups was more pronounced in the D. galeata × cucullata hybrid compared to D. galeata, whereas selection intensity was weaker. These results are discussed with respect to stability of clonal groups, multiple hybridizations and selective constraints.     

Experimental interspecific hybridization in Daphnia

Hybridization is a common phenomenon in Daphnia (Cladocera; Anomopoda); interspecific hybrids have been found between several species and hybrids are found in many European lakes. Although much information on the morphology, ecology and genetics of hybrids is available, little is known about the level of reproductive isolation among species or about the relative fitness of hybrids and parental species. In order to facilitate studies on differentiation and speciation processes and comparative experimental studies on hybrids and recombinant genotypes, we present the first successful laboratory crossing experiments of two different Daphnia species, D. galeata and D. cucullata. Males and sexual females from two D. galeata and two D. cucullata clones were reciprocally crossed, juveniles hatched from resting eggs and reared until maturity. Hatching and juvenile survival rates of hybrids were relatively low (12.1% and 24%, respectively). D. galeata and D. cucullata clones vary in their level of successful interspecific matings and in the number of subsequent offspring. In general, hybrid crosses between D. cucullata females and D. galeata males were more successful than reciprocal crosses.     

Cyclomorphosis as a factor explaining success of a Daphnia hybrid in Tjeukemeer

Recent studies have shown that Daphnia hybrids are intermediate to their parental species for several life history traits, and that they combine advantageous traits of the parental species, thereby decreasing their risk of being preyed upon by planktivorous fish. In this study D. galeata, D. cucullata and their interspecific hybrid are compared with respect to cyclomorphosis and juvenile growth as a potential mechanism to avoid invertebrate predation. Helmets and tail spines are known to reduce predation risk, whereas fast juvenile growth reduces the period that Daphnia are vulnerable to predation. In laboratory cultures, I tested the hypothesis that, with regard to cyclomorphosis, juvenile hybrids are more comparable to the juveniles of D. cucullata, and with respect to growth rate, they are more comparable to D. galeata. The hybrid did not differ significantly from D. galeata in the time needed to reach 0.9 mm body length. In contrast, the relative spine and helmet length of juvenile hybrids were more comparable with those of D. cucullata, whereas in adult instars these characters were more similar to D. galeata. Thus during the first juvenile instars, the hybrids combine the relative long helmet and spine of D. cucullata, with the faster growth of D. galeata. This combination of characteristics might reduce hybrid vulnerability to invertebrate predation in field situations.     

Impact of fish predation on coexisting Daphnia taxa: a partial test of the temporal hybrid superiority hypothesis

Fish predation was tested as a factor mediating the coexistence of Daphnia taxa in the shallow, hypertrophic Lake Blankaart. Naturally co-occurring populations of D. galeata and the hybrid D. galeata x cucullata were subjected to different levels of fish predation in in situ enclosures. In control enclosures without fish, the largest taxon D. galeata rapidly became dominant over the intermediate sized D. galeata x cucullata, mainly as a result of higher birth rates. In enclosures with fish, population densities of D. galeata dropped relative to D. galeata x cucullata, due to higher mortality rates. These results are in concordance with the `temporal hybrid superiority hypothesis', and can be explained by a higher vulnerability of the large and more conspicuous D. galeata to the size selective predation exerted by visually hunting planktivorous fishes. After approximately one month, however, population growth rates of D. galeata and D. galeata x cucullata in the enclosures with fish converged, due to a relative reduction in the mortality rate of D. galeata. This suggests that, in the presence of fish, D. galeata may co-exist with hybrids due to a decrease in its relative vulnerability to visual predation with time. Indeed, both D. galeata and the hybrid showed strong reductions in adult body size in the enclosures with fish, but this size reduction tended to be stronger in D. galeata than in D. galeata x cucullata. In addition, turbidity increased in the enclosures with fish and may additionally have reduced the relative advantage of D. galeata x cucullata with regard to mortality caused by visual predation.     

Resource depression in Daphnia galeata, Daphnia cucullata and their interspecific hybrid: life history consequences

In this study, the effect of the food concentration on severallife history parameters of Daphnia galeata, Daphnia cucullataand the hybrid between these two species was examined. The foodconcentration had a significant effect on both growth and reproductionof all three taxa. Mortality was highly species specific, andto a lesser extent dependent on the food concentration. Changesin life history parameters resulted in changes in the intrinsicrate of population increase (r). The food dependence of thedifferent species was found to be different. Daphnia cucullatahad a relatively constant and low r. The r values for the hybridvaried most, with low values compared with the parental specieswhen grown at low food levels and relatively high values athigher food concentrations. Our results suggest that when foodconcentrations are high the hybrid will have a selective advantageover both parental species, but that at lower food levels D.galeatawill have an advantage over both D.cucullata and the hybrid.     

Life history patterns of parental and hybrid Daphnia differ between lakes

1. We investigated whether Daphnia galeata × hyalina hybrids of Lake Constance and Lake Greifensee show the same pattern of life history parameters as previously reported for D. galeata × cucullata hybrids and whether such a pattern is consistent between Daphnia populations from those two lakes. 2. Hybrids in Lake Constance were intermediate in size compared with the parental species. Hybrids in Lake Greifensee were smaller than D. galeata. The intrinsic growth rate (r) of hybrids from Lake Constance was not significantly different from the faster growing parental taxon D. galeata. However, r of hybrids from Lake Greifensee was significantly lower than that of D. galeata. 3. The observed juvenile body length differences between the taxa varied with the clutch number. The first clutch juvenile lengths of the three taxa did not differ for Lake Constance. First clutch juveniles of Lake Greifensee D. galeata were smaller than hybrid first clutch juveniles. The third clutch juvenile length did not differ between taxa from Lake Greifensee, but D. galeata juveniles from Lake Constance were bigger than those of D. hyalina. 4. The life history pattern found in Lake Constance corresponds to previous findings from other studies. The hybrids in this lake combine the faster population growth of one parental species with a relatively small size. In the case of Lake Greifensee hybrids, the relatively large size of first clutch juveniles and the small size of the adults could be interpreted as dual adaptations to invertebrate and fish predation. We speculate that the lower population growth rate of the hybrids is a trade‐off for this twofold protection.     

Plasticity in filtering screens of Daphnia cucullata×galeata hybrids and parental species at two food concentrations

The coexistence of Daphnia cucullata × galeata hybrids with the parental species D. galeata and D. cucullata was investigated by measuring areas and mesh sizes of filtering structures of these herbivorous zooplankton taxa cultivated at low and high food concentrations. The clearance rates and somatic growth rates were also determined. When reared at low food concentration, all taxa had larger filtering areas. Larger filtering areas also resulted in higher clearance rates. Differences between taxa in both filtering area and clearance rate were caused mainly by interspecific size differences. Hybrids had the largest absolute mesh sizes, and the parental species had smaller mesh sizes. Hybrids also showed heterosis in somatic growth rate at high food concentration. The observed taxon-specific differences in mesh size and somatic growth rate contribute to resource partitioning between the taxa and thus to their successful coexistence in lakes. Received: 1 March 1999 / Accepted: 25 May 1999     

Interspecific hybridization betweenDaphnia hyalina,D. galeata,andD. cucullata and seasonal abundances of these species and their hybrids

The three cladoceran speciesDaphnia hyalina, D. galeata, andD. cucullata frequently coexist in the lakes of northern Germany. Although there are some problems in distinguishing them morphologically, they are easily determined by gelelectrophoresis: each species carries a different allele at the glutamate oxaloacetate transaminase (GOT) locus. Animals morphologically intermediate between two species are heterozygous for the alleles carried by the species they resemble. This pattern is in agreement with the findings at other loci, where also diagnostic alleles exist. These findings are most easily explained by interspecific hybridization between the three species. No evidence is found for backcrosses involving hybrids ofD. cucullata, whereas some backcrosses betweenD. hyalina, D. galeata, and their hybrids are found in some lakes. In four lakes the seasonal abundances of the three species and their hybrids are determined.     

The possible origin ofDaphnia cucullata procurva Poppe 1887 in the lakes of the Pomeranian Lakeland by hybridization in the past

Besides the genusBosmina, the genusDaphnia offers considerable taxonomic difficulties due to the existence of a very great number of different morphotypes and their intergrades. Especially the morphotypes clustering aroundDaphnia galeata Sars, 1864,D. hyalina Leydig, 1860, andD. cucullata Sars, 1862 offer a bewildering picture. In the last years an attempt has been made to understand this phenomenon mainly as the result of hybridization and colonization of new biotopes by populations with hybridogenetic polymorphism and genotypic diversity (founder effect). Now it will be suggested on a morphological base thatD. cucullata procurva Poppe, 1887, a unique and aberrant formtype restricted to few lakes along the river Brda in Poland, is probably an old and stabilized hybrid originating from interspecific hybridization betweenD. galeata andD. cucullata.     

Life-history variation in a hybrid species complex ofDaphnia

Summary Life-history variation was examined among members of theDaphnia longispina group, which consists ofD. galeata, D. hyalina, D. cucullata, and hybrids. Factorial experiments were conducted at two temperatures (14° and 20° C) and two food concentrations (0.2 and 1.0 mg Cl⁻¹). Differences in life-history features (size at maturity, age at first reproduction, size of first clutch, offspring size in first clutch) under the different environmental conditions were assessed among eightDaphnia clones, which represented members of this species complex. Significant differences between parentals and hybrids for most life-history features were observed under various treatments; generally, hybrid clones showed intermediate life-history traits when compared with parentals. When comparisons were made among clones within a given species (i.e.D. galeata, D. galeata xcucullata, D. cucullata), clonal differences were also noted for certain life-history traits. The data are discussed with reference to the formation and maintenance of hybrid species complexes in nature. This paper is dedicated to the memory of Hans Georg Wolf, who died suddenly in May 1990 at the age of 39 years.     

Spatial and temporal patterns of sexual reproduction in a hybrid Daphnia species complex

Evidence for extensive interspecific hybridization among speciesof the genus Daphnia has been accumulating on a global scale.Although there is evidence for limited gene flow between taxavia hybridization, many species still maintain discrete morphologicaland molecular characteristics. We studied temporal and spatialpatterns of sexual reproduction within the Daphnia galeata–hyalina–cucullatahybrid species complex in a lake (Plußsee), located innorthern Germany. Allozyme electrophoresis allowed us to trackseasonal changes in taxon composition as well as the quantificationof back-crosses. Sexually-reproducing animals (ephippial femalesand males) were mainly found in autumn. The simultaneous presenceof sexual morphs of D. galeata and D. galeata x hyalina withthe dominant D. hyalina taxa makes recent hybridization, aswell as back-crossing, plausible. Males and ephippial femalesof D. hyalina were not back-crossed as were the parthenogeneticfemales. The low number of sexual clones of the hybrid D. galeatax hyalina might reflect its reduced fertility, although thesefew clones were detected in high densities. Only hybrid-clonesthat had a back-cross genotype (towards D. hyalina) exhibitedephippial females and males. This indicates that male and ephippialfemale production within the Daphnia taxa is not random, whichmight increase the chance for the parental Daphnia species toremain distinct.     

Seasonal dynamics of metabolic activity of the Daphnia community in Lake Bled (Slovenia)

Seasonal changes of the community composition, oxygen consumption (R) and respiratory electron transport system (ETS)-activity of the Daphnia community living in Lake Bled (Slovenia) were studied between January and December 1998. The ETS activity of ovigerous Daphnia females at in situ temperature ranged from 3.27 l O₂ mg dw^–1 h^–1 in February to 20.91 l O₂ mg dw^–1 h^–1 in July. Respiration rates at in situ temperature varied from 4.04 l O₂ mg dw^–1h^–1 in December to 18.68 l O₂ mg dw^–1 h^–1in July. The influence of four factors (temperature, body size, fecundity, genetic differences) on the metabolism were investigated. Both ETS activity and respiration rate significantly correlated with temperature. The proportion of hybrid D. cucullata× galeata in Daphnia community correlated significantly with respiration rate at in situtemperature and ETS activity at standard temperature also. ETS activity and respiration rate showed no significant correlation with body size and the fecundity of Daphnia, whereas ETS activity in D. hyalina × galeata and D. cucullata× galeataseparately correlated with body size. ETS activity of D. hyalina × galeata also was correlated with fecundity. Hybrid D. hyalina× galeata had up to one third lower ETS activity than D. cucullata× galeata. The mean ETS/R ratio in the Daphnia community was 1.16±0.28 (N= 12). The ETS/R ratio did not correlate significantly with temperature, body size, fecundity or the proportion of D. cucullata× galeatain the Daphnia community. Laboratory experiments showed that both hybrids had similar ETS/R ratios.     

Sexual reproduction in Daphnia: interspecific differences in a hybrid species complex

To investigate whether reproductive variation in the Daphnia galeata-cucullata-hyalina hybrid species complex can explain the occurrence of hybrids and backcrosses, a total of 43 clones from three north German lakes were tested for allocation to sexual reproduction under equal stress conditions. Six replicates per clone were followed until the seventh adult instar. I used the following cues to promote sexual reproduction: short photoperiod, water from a crowded Daphnia culture, fish-conditioned water and low food concentration. For each animal, clutch size and clutch sex were recorded. Ephippia, which were empty since the animals were cultured individually, were only produced by D. cucullata and D. cucullata x hyalina (26% and 6% of the broods, respectively), whereas almost all taxa produced males (the range was 2–15%). Intraspecific variation for male and ephippial production was also found. The fact that the taxa tested show different responses to the stimuli of-fered may indicate that there is reproductive isolation between them. This is supported by field data from the Tjeukemeer (The Netherlands) which shows that D. galeata mostly produces ephippia in spring and D. cucullata in autumn. The presence of hybrids with ephippia in both seasons, however, shows that backcrossing is also possible.     

Inter-specific hybridization underlies phenotypic variability in Daphnia populations

Summary In the glacial lakes of the Palaearctic three species of Cladocera commonly coexist: Daphnia hyalina, D. galeata, and D. cucullata. Frequently these populations contain not only animals which are morphologically typical for the species but also individuals of an intermediate phenotype. Electrophoretic investigations of allozyme-patterns in morphologically typical individuals reveal that each species is fixed for a different allele at the GOT locus. Morphologically intermediate animals are heterozygous for the alleles of the two species which they resemble. The allelic pattern at other loci is also consistent with the assumption that morphological intermediates are formed via interspecific hybridization. Very few backcrosses between galeata-hyalina hybrids and their parent species are found, and there is no indication of gene flow between D. cucullata and the other species.     

Competitive ability of Daphnia under dominance of non-toxic filamentous cyanobacteria

It is generally assumed that Daphnia is more susceptible to the inhibitory effects of filamentous cyanobacteria than small cladocerans since daphnids have a larger gape size and filtrate the filaments, whereas small cladocerans do not. This study addresses the question whether food limitation has the potential to modify this scenario of cladoceran response to dominance of non-toxic filamentous cyanobacteria. Daphnia galeatawas grown under limited (0.1 mg C l^–1) and unlimited concentrations (1.0 mg C l^–1) of high-quality food algae both in the absence/presence of non-toxic filamentous Aphanizomenon flexuosum. As the effects of these cyanobacteria on D. galeatawere positive under food limiting conditions and negative at the high food density, it was concluded that D. galeatawas mainly affected by nutritional quality due to its ability to ingest the filaments, while mechanical interference with food collection was not important. In competition experiments between D. galeataand Bosmina longirostris, D. galeatawas the dominant species at regular additions of food (1.0 mg C l^–1) in the absence of Aphanizomenon. In the presence of these cyanobacteria, D. galeatawas inhibited during the first days of the experimental period. However, the negative effect at the initially high food density was outweighed by nutrition at food limiting conditions and the outcome in competitive dominance was not changed. The results demonstrate that the ability of D. galeata to ingest large-sized non-toxic cyanobacteria can be considered as advantageous under food limiting conditions.     

Daphnia Galeata × D. Longispina Hybrids in Western Norway

We describe the occurrence of D. galeata×longispina hybrids in two lakes of western Norway. Parental species and interspecific hybrids were characterised by both nuclear and mitochondrial molecular markers. In one of the populations, hybrids were shown to dominate the population over several years. A few individuals in both populations were probably not F1 hybrids, but possibly backcrosses or F2 hybrids. Most (possibly all) F1 hybrids were of D. galeata maternal origin. In addition, interspecific hybrids could be identified based on morphological characters, which were intermediate between the parental species. Interspecific hybridisation between these two species is remarkable, since they are distantly related.     

Estimating Competition in Cladocerans Using Data on Dynamics of Clutch Size and Population Density

Negative correlations between clutch size and population density are proposed to be considered as indices of intra- and interspecific competition in cladocerans if they are revealed while analyzing population dynamics and clutch size and time lags are taken into account. The proper correlation analysis of summer populations of Diaphanosoma brachyurum, Bosmina coregoni, Daphnia cucullata and D. galeata from mesotrophic Lake Glubokoye (Moscow Region) in 1975, 1978, and 1979 indicates the important role of competition of both types for the community studied. High niche overlap in food and space in the four populations was also observed.     

On the taxonomy of theDaphnia hyalina-galeata complex (Crustacea: Cladocera)

Populations of theDaphnia hyalina-galeata complex from Central, North and South Europe have been compared morphologically. The main purpose of this investigation is delimitation of the critical speciesDaphnia galeata, based on a thorough examination of the original materials from G. O. Sars' collection, and taking into account hitherto overlooked or insufficiently appreciated characters. According to their morphology and ecology,Daphnia hyalina, Daphnia galeata andDaphnia cucullata have to be treated taxonomically as separate species. In view of the short and high antennula mound and other morphological characteristics,Daphnia gracilis Hellich andDaphnia hyalina lacustris sensu Lilljeborg belong to the speciesDaphnia galeata. In the common range ofDaphnia galeata andDaphnia cacullata there occurs quite frequently an intermediary form, which according to genetic evidence is a hybrid of these two species. Although apparently this hybrid form is stabilized genetically to a large extent and is capable of identical reproduction, it should not be considered as a species in the usual sense.The present work intends to put the notoriously confused systematics of theDaphnia hyalina-galeata complex on a firm basis. It concludes with a key, which should enable also non-specialists to identify uniquely the three species and the hybrid form in question.     

Identifying hybridizing taxa within the <Emphasis Type="Italic">Daphnia longispina</Emphasis> species complex: a comparison of genetic methods and phenotypic approaches

Daphnia galeata Sars, D. longispina O. F. Müller and D. cucullata Sars (Crustacea: Cladocera) are closely related species which often produce interspecific hybrids in natural populations. Several marker systems are available for taxon determination in this hybridizing complex, but their performance and reliability has not been systematically assessed. We compared results from identifications by three molecular methods. More than 1,200 individuals from 10 localities in the Czech Republic were identified as parental species or hybrids by allozyme electrophoresis and the analysis of the restriction fragment length polymorphism of the internal transcribed spacer (ITS-RFLP); over 440 of them were additionally analyzed and identified by 12 microsatellite loci. Identification by microsatellite markers corresponded well with allozyme analyses. However, consistent discrepancies between ITS-RFLP and other markers were observed in two out of 10 studied localities. Although some marker discrepancies may have been caused by occasional recent introgression, consistent deviations between ITS-RFLP and other markers suggest a long-term maintenance of introgressed alleles. These results warn against its use as a sole identification method in field studies. Additionally, we quantitatively evaluated the discriminatory power of geometric morphometric (elliptic Fourier) analysis of body shapes based on photos of over 1,300 individuals pre-classified by allozyme markers. Furthermore, a randomly selected subset of 240 individuals was independently determined from photos by several experts. Despite a tendency for morphological divergence among parental Daphnia species, some taxa (especially D. galeata, D. longispina, and their hybrids) substantially overlapped in their body shapes. This was reflected in different determination success for particular species and hybrids in discriminant analysis based on shape data as well as from photographs.