Independent life history evolution between generations of bivoltine species: a case study of cyclical parthenogenesis

Successive generations of bi- and multivoltine species encounter differing biotic and abiotic environments intra-annually. The question of whether selection can independently adjust the relationship between body size and components of reproductive effort within successive generations in response to generation-specific environmental variation is applicable to a diversity of taxa. Herein, we develop a conceptual framework that illustrates increasingly independent life history adjustments between successive generations of taxa exhibiting complex life cycles. We apply this framework to the reproductive biology of the gall-forming insect, Belonocnema treatae (Hymenoptera: Cynipidae). This bivoltine species expresses cyclical parthenogenesis in which alternating sexual and asexual generations develop in different seasons and different environments. We tested the hypotheses that ecological divergence between the alternate generations is accompanied by generational differences in body size, egg size, and egg number and by changes in the relationships between body size and these components of reproductive effort. Increased potential reproductive effort of sexual generation B. treatae is attained by increased body size and egg number (with no trade-off between egg number and egg size) and by a significant increase in the slope of the relationship between body size and potential fecundity. These generation-specific relationships, interpreted in the context of the model framework, suggest that within each generation selection has independently molded the relationships relating body size to potential fecundity and potential reproductive effort in B. treatae. The conceptual framework is broadly applicable to comparisons involving the alternating generations of bi- and multivoltine species.     

Avian egg collections: museum collection bias driven by shape and size

Avian eggs exhibit substantial intra- and interspecific variation in shape, size and colour. Considerable efforts have been made to better understand the evolutionary drivers behind such variation, often using museum egg collections. Usually it is assumed that museum collections accurately represent the variation seen in natural populations, but this may not be the case if there is collection bias. Collection bias may lead to the over-representation of certain egg traits in collections, due to the aesthetic (or other) preferences of collectors. The aim of this study is to begin to look for the occurrence of potential collection bias in museum egg collections by comparing three shape indices (pointedness/asymmetry, elongation and polar asymmetry) and egg volume between subsets of eggs in museum collections with those of recently sampled eggs in the field for three different bird species: common guillemot Uria aalge, razorbill Alca torda and northern fulmar Fulmarus glacialis. We found no evidence of collection bias in our sampled razorbill and northern fulmar museum collection eggs, but some evidence for a bias in sampled museum collection eggs of common guillemots. Since the guillemot's egg differs from most bird eggs in being pyriform, we suggest that collection bias by historic egg collectors may be more prevalent in species with extreme egg traits. Researchers using museum egg collections to examine questions relating to egg shape should be aware of collection bias risks and consider how to minimise the effect of these possible biases on accumulated datasets.     

Calculating egg volume when shape differs: when are equations appropriate?

ABSTRACT Egg volume is often calculated from length and breadth, assuming little variation in egg shape within species. However, egg shape may vary among females, over time, or within clutches. If this variation is not predictable, volume should be estimated using another method. For example, in some species, egg shape changes consistently with laying order and volume can be estimated using laying‐order specific equations. We measured the length, breadth, volume, and mass of 249 Magellanic Penguin (Spheniscus magellanicus) eggs and regressed volume on length and breadth for first and second eggs separately. Differences between measured and calculated volume averaged <1% for both eggs. Using linear measurements, we calculated egg volume for 7085 clutches from 1983 to 2006. First and second eggs had similar calculated volumes (P > 0.05) in 19 of 24 yr; when they differed, the second egg was larger. In contrast, using single equations typically employed to compute egg volume, we erroneously concluded that first eggs were usually (20 of 24 yr) significantly larger than second eggs. Our regression equations should be applicable to other Spheniscus penguins because ratios of elongation coefficients (length divided by breadth) of first and second eggs are similar among these species. In other species of birds where egg shape changes with laying order, the volume of a sample of eggs should be measured to develop regression equations specific to the species and laying order. Slight variation in egg volume can have important evolutionary and ecological implications that would be erroneously interpreted without field tests to measure volume.     

Microtubules and control of insect egg shape

This study evidence for tension transmission by microtubules and desmosomes in the follicular epithelium during anisometric growth of certain insect eggs. Most insect oocytes, and the follicles which surround them, grow anisometrically as they assume shapes which approximate to those of long prolate spheroids. Surface growth is most rapid in directions which parallel the polar axis of an oocyte and slowest in circumferential directions at right angles to this axis. The longitudinal axes of microtubule bundles in follicle cells of the gall midge Heteropeza and the cockroach Periplaneta are oriented circumferentially with respect to the surfaces of developing eggs and at right angles to the polar axes of eggs. At cell boundaries, the tubules appear to be attached to spot desmosomes. It is suggested that microtubules and desmosomes form a mechanical continuum throughout a follicular epithelium which transmits tensile forces around the circumference of a growing egg. Follicular resistance to circumferential expansion may be largely responsible for defining the elongate form of insect eggs.     

The evolution of egg shape in birds: selection during the incubation period

A recent broad comparative study suggested that factors during egg formation – in particular ‘flight efficiency’, which explained only 4% of the interspecific variation – are the main forces of selection on the evolution of egg shape in birds. As an alternative, we tested whether selection during the incubation period might also influence egg shape in two taxa with a wide range of egg shapes, the alcids (Alcidae) and the penguins (Spheniscidae). To do this, we analysed data from 30 species of these two distantly related but ecologically similar bird families with egg shapes ranging from nearly spherical to the most pyriform eggs found in birds. The shape of pyriform eggs, in particular, has previously proven difficult to quantify. Using three egg‐shape indices – pointedness, polar‐asymmetry and elongation – that accurately describe the shapes of all birds’ eggs, we examined the effects of egg size, chick developmental mode, clutch size and incubation site on egg shape. Linear models that include only these factors explained 70–85% of the variation in these egg‐shape indices, with incubation site consistently explaining > 60% of the variation in shape. The five species of alcids and penguins that produce the most pyriform eggs all incubate in an upright posture on flat or sloping substrates, whereas species that incubate in a cup nest have more spherical eggs. We suggest that breeding sites and incubation posture influence the ability of parents to manipulate egg position, and thus selection acting during incubation may influence egg‐shape variation across birds as a whole.     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

A comparison of life history traits of sexual and asexual strains of the parasitoid wasp,Lysiphlebus fabarum (Braconidae: Aphidiinae)

1. This study examined biological characteristics of sexual and asexual strains of the parasitoid wasp, Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). 2. Strains were reared in different instar hosts (the black bean aphid, Aphis fabae Scopoli) under identical environmental conditions (21 °C, 65–75% RH, and LD 16:8 h). 3. Results showed that the second instar of the aphid is the most suitable growth stage for both strains, as the wasps that emerged from the second instar hosts were larger, more fecund, and had larger egg size. Trade‐offs between the fitness components of the parasitoid were clearer when the parasitoids were reared in suboptimal instars. 4. According to the results, sexual females emerged around 1 day earlier and lived around 0.5 day less than asexual females. Also, sexual females emerged with a lower initial egg load, although these wasps tend to have larger eggs than asexual females. Asexual females may enjoy greater longevity and higher developmental plasticity which suggests a higher degree of synchronization with pest population dynamism. 5. The results suggest that sexual wasps, in contrast to asexual wasps, invest more in egg size than in egg load. This study suggests strain‐specific adaptations of L. fabarum to different instars of the black bean aphid by which the allocation of nutritional resources to various functions differs between strains. 6. Furthermore, differences in life history traits between strains can greatly influence the population dynamics of each strain, and hence their effectiveness in suppressing pest populations.     

Genetic variability and transgenerational regulation of investment in sex in the monogonont rotifer Brachionus plicatilis

In cyclical parthenogens such as aphids, cladocerans and rotifers, the coupling between sexual reproduction and the production of resting stages (diapausing eggs) imposes strong constraints on the timing of sex. Whereas induction of sex is generally triggered by environmental cues, the response to such cues may vary across individuals according to genetic and nongenetic factors. In this study, we explored genetic and epigenetic causes of variation for the propensity for sex using a collection of strains from a Spanish population of monogonont rotifers (Brachionus plicatilis) in which variation for the threshold population density at which sex is induced (mixis threshold) had been documented previously. Our results show significant variation for the mixis threshold among 20 clones maintained under controlled conditions for 15 asexual generations. The effect of the number of clonal generations since hatching of the diapausing egg on the mixis ratio (proportion of sexual offspring produced) was tested on 4 clones with contrasted mixis thresholds. The results show a negative correlation between the mixis threshold and mixis ratio, as well as a significant effect of the number of clonal generations since fertilization, sex being repressed during the first few generations after hatching of the diapausing egg.     

Egg size manipulation in the migrant skipper, Parnara guttata guttata (Lepidoptera: Hesperiidae), in response to different host plants

Female adults of the migrant skipper, Parnara guttata guttata, lay different-sized eggs on different host plants in different generations. Moreover, P. g. guttata maintains large egg size variation either in the population or in the individual. Why such phenotypic plasticity in egg size is maintained has not been clarified. In the present study we performed a series of experiments to verify whether or not females of P. g. guttata discriminate between the different host plants, i.e., rice plant Oriza sativa in the first and second generations and cogon grass Imperata cylindrica in the third (overwintering) generation and manipulate egg size accordingly on these host plants. When a caged female was allowed to lay eggs alternatively on soft-leafed rice plant and tough-leafed cogon grass, the size of the eggs laid on cogon grass was significantly larger than that on rice plant. When a caged female was allowed to lay eggs on the two host plants that were supplied on alternate days, the size of eggs laid on cogon grass was also significantly larger than that on rice plant. A preliminary experiment using crude extract from the plants suggested that females did not manipulate egg size in response to chemical stimulants alone. The skipper female was able to lay different-sized eggs instantaneously after assessing the host plant. However, the reaction norm to different host plants differed among females. Eggs of various sizes were matured in each ovariole, and egg size variation at the lowest part of the ovariole ranged from the size of the larger eggs laid on cogon grass to that of the smaller eggs laid on rice plant, although how the female chose the appropriate-sized egg at each occasion is unknown.     

The optimal shape of avian eggs

1. The shape of avian eggs is often explained by involving the mechanical properties of eggshell such as resistance to breakage or invoking physiological forces operating during egg development.
2. Here we take a different approach and investigate the efficient use of space. According to this approach the optimal egg shape is the one that produces the most compact fit under the incubating parent.
3. We extend the model of Andersson (1978) and use a numerical technique to investigate egg shapes in clutches of 1 to 10 eggs. In our model the shape of eggs is described by four parameters in a two-dimensional space. These parameters are free to vary – but eggs cannot be concave.
4. The optimal egg shape for each clutch size was found by a genetic algorithm.
5. The model predicts that egg shape should depend on clutch size. In particular, if the clutch consists of one egg then this egg should be spherical; whereas in clutches of two or three eggs the eggs should be biconical. In clutches of four the eggs should be pointed. The model also predicts that in clutches of over seven eggs the optimal egg shape should be approximately spherical.
6. These predictions are valuable because they point out that some of the variation in avian egg shapes may be explained solely by the efficient use of the brood patch area of the incubating parent.     

Life history of the sand fly vector Lutzomyia cruciata in laboratory conditions

Lutzomyia cruciata Coquillet (Diptera: Psychodidae: Phlebotominae) is a potential vector of Leishmania sp.; its geographical distribution in Mexico is widespread, but its life history is unknown. The present study gives relevant information on the life cycle, morphology, survival and reproduction of Lu. cruciata observed over successive generations under laboratory conditions. Seven successive generations were produced. A total of 975 adults were obtained in a sexual proportion of 1.1 : 1 (female : male). Each Lu. cruciata female produced 20.7 eggs and 1.9 adults, approximately, with a proportion of eggs per female of 2.7% (first generation) and 21.3% (second generation). The life cycle of Lu. cruciata, from egg to adult, occurred in 52.7 ± 0.52 days. The largest percentage of mortality occurred during the egg stage (48.5%) and the first larval instar (26.5%), whereas in the pupal stage mortality was the lowest (9.1%). Lutzomyia cruciata exhibits sexual dimorphism based on size, which is exhibited as of the second larval instar, males being smaller than females. The maximum survival of females and males was 10 and 15 days, respectively. An overview of the immature stages of the species made with an electronic scanning microscope is included. This paper contributes basic information on aspects of Lu. cruciata that were previously unknown related to its life history.     

Modelling intraspecific resting egg shape variation in a freshwater fairy shrimp Tanymastix stagnalis (L., 1758) (Crustacea, Branchiopoda)

The shape of the resting eggs of a large branchiopod crustacean, the Anostraca Tanymastix stagnalis , is represented very accurately by analytical expressions. The occurrence of atypical shape of some T. stagnalis eggs may be viewed as a simple change of the analytical expression describing the usual egg shape. Their unusual shape may be explained by a higher embryo volume within an envelope of a given size. Biological implications are briefly discussed and hypothesized in an evolutionary point of view.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 55–60.     

Phenotypic plasticity of reproductive effort in a colonial ascidian,Botryllus schlosseri

Phenotypic plasticity is the capability of a genotype to produce different phenotypes in different environments. Previous studies have indicated phenotypic variability in asexual, male, and female reproduction in Botryllus schlosseri, a hermaphroditic, colonial ascidian, but not explicitly tested for genotype by environment interactions that indicate genetic variation in plastic responses. Consequently, clones derived from an estuarine population were deployed at their native site and a warmer, higher productivity site 10 km up-river. Male reproduction was assayed by testis size, female reproduction by the number of eggs produced, and asexual reproduction by colony growth rate. To test for ontogenetic effects, data were collected from two different generations of zooids born in the field. Analyses of variance indicated plasticity in asexual and female reproduction during the first zooid generation and plasticity in all three traits during the third zooid generation. Reaction norms varied significantly among genotypes in direction and magnitude for asexual reproduction at both times, implying that selection on asexual reproduction is weak. Sperm production during the third zooid generation was significantly lower at the nonnative site, but there was no genotype by environment interaction. The reaction norms for female reproduction varied significantly among genotypes in direction and magnitude during the first zooid generation, but only varied in magnitude during the third generation, with egg production being higher in all genotypes at the nonnative site. Comparisons of weighted frequency distributions between sites demonstrated that differences in egg production in the third generation were due to increases in the proportion of reproductive zooids within a colony. The greater emphasis on female reproduction at a site associated with higher food availability and temperature, and the greater emphasis on male reproduction at a colder, food-limited site, supports predictions from sex allocation theory.     

Characterization of a sperm lysin of Volvox carteri

Summary A cell-wall degrading enzyme has been isolated from mature sperm packets of the green flagellate Volvox carteri (Poona strain). This sperm lysin (S-lysin) is a Ca²⁺-dependent protease of 34 kDa with an essential serine group in its active centre. Neither SH group-blocking reagents nor transition metal chelators inhibit its action. S-lysin degrades the hydroxyproline-rich glycoprotein structures of the cell walls of sheath cells and gonidia (eggs) of vegetative and sexual spheroids in a characteristic manner. In asexual spheroids the somatic envelope is totally disintegrated, whereas in sexual spheroids pores are formed by local lysis at sites of adjacent eggs. Although S-lysin is very similar to the G-lysin of the closely related Chlamydomonads, it is species specific and does not attack the mother or daughter cell walls of Chlamydomonas reinhardtii. S-lysin resembles the aerosin of animal sperm cells in some aspects of its action.Dedicated to Professor Richard C. Starr on the occasion of his 65th birthday. He called the piper and gave the tune     

Extreme tolerance to environmental stress of sexual and parthenogenetic resting eggs of Eucypris virens (Crustacea,Ostracoda)

1. The freshwater ostracod (Ostracoda), Eucypris virens, is commonly found in European temporary pools, where its long‐term persistence completely relies on the build‐up of resting egg banks. Extreme tolerance of dormant eggs and seeds is widely assumed, but freshwater ostracod eggs are relatively poorly studied. The study of ostracod resting eggs is of particular relevance as it may yield the key to understanding the distribution of the sexes in many species capable of both sexual and asexual reproduction. 2. We assessed the tolerance of dried resting eggs produced by females originating from three populations with males and three all‐female E. virens populations. Hatching time and success was compared between control eggs and eggs exposed to one of seven ecologically relevant stressors: digestive enzymes, high salinity, deep freezing, hydration, UV‐B radiation, hypoxia and insecticide treatment. 3. None of the stressors reduced significantly the viability of either sexual or asexual eggs. When compared with the reproductive mode–specific controls, exposure to UV‐B radiation had a mild impact on the survival of sexual and asexual eggs (?16.8 and ?22.4%, respectively), but this was only significant for asexual eggs. These results point to an extreme tolerance of E. virens resting eggs and have important implications for the ecology and evolution of the species. 4. The timing of hatching was not affected by the stress treatment, except for UV‐B radiation. A marginally significant delay in hatching response was observed for UV‐B‐radiated eggs when compared to the overall mean, but this treatment effect was absent when compared with the reproductive mode–specific controls. 5. The populations with males produced eggs that hatched on average earlier (?1.5 days at 17 °C) and were more successful (+26%) than asexual eggs. Due to the limited number of populations and the population‐specific origin and age of the eggs, the possibility due to the differences in age and origin of the resting eggs, or to variations in local conditions, cannot be ruled out.     

The role of parthenogenesis in the biology of two species of mayfly (Ephemeroptera)

1. From a single founder virgin female of each species, nine and seven successive parthenogenetic generations of Cloeon dipterum and Cloeon simile, respectively, were reared: all offspring were female. Eggs were removed from final instar nymphs, subimagos and virgin imagos of each generation and their development assessed. The life cycles of 487 individual C. dipterum and 315 C. simile were recorded, together with details of growth rate, egg production and adult size of these and other representatives of each generation. In order to distinguish between the effects of parthenogenesis and the effects of culture conditions, fertilized eggs of both species were reared under the same laboratory conditions. 2. Fewer unfertilized than fertilized eggs hatched. There was no consistent trend in the percentage hatch in successive parthenogenetic generations. In both species the time taken for parthenogenetic individuals to complete a generation varied considerably, and no relationship was found between generation length and the number of parthenogenetic generations that had passed, the developmental stage of the donor, or the time taken for the eggs to hatch. After 50 weeks there was, in both species, an overlap of up to six generations. The number of eggs produced by both species was significantly greater in the first parthenogenetic generation than in later generations but the numbers for later generations lie within the recorded range of egg number in imagos captured in the field. 3. To find if parthenogenetic individuals occur in the field, the sex ratios of last instar nymphs and subimagos of C. simile were measured in samples collected over 13 successive years from a set of small isolated pools. There was a female bias both in winter and at the start of the emergence season. It is possible that, when mature nymphs and emerging subimagos are damaged by predators, the eggs which are released from them survive and develop. 4. Mature, egg-containing nymphs of both species were present in the field throughout the year, although their numbers were small at the beginning of winter. 5. Oviposition by imagos captured from mating swarms and by virgin imagos, of both species, was recorded for the first time, showing that C. dipterum is not always ovoviviparous. It is suggested that early instar nymphs occurring in mid-winter come not only from unfertilized eggs released from injured nymphs and subimagos, but also from fertilized eggs laid in autumn.     

Egg size, egg composition and reproductive success in the Oystercatcher Haematopus ostralegus

We investigated the relationship between egg size and composition and their subsequent effects on hatching and fledging success in Eurasian Oystercatchers Haematopus ostralegus on the island of Schiermonnikoog (53̀30'N, 06̀10'E) in the Dutch Wadden Sea between 1986 and 1990. Egg size variation was considerable. The ratio in egg volume of the largest over the smallest egg was more than 1.5 in each of five years. Differences between females accounted for, on average, 61% of the total variance of egg volume. Individual females produced similarly sized eggs from one year to another. Nevertheless, average egg volume per clutch declined by 0.2 cm³ per year as females aged, but this explains little of the observed variation. Female size and food supplementation had no significant effect on egg volume. In absolute terms, large eggs contain more lean dry matter and lipid than small eggs, but the proportion of both constituents decreases with egg size. Consequently, the combustible energy content of eggs increases less than proportionally with egg size. Hatchability averaged 87% and was not correlated with egg volume. Hatchling weight increased with egg size, averaging 65% of fresh egg weight. Chick survival until fledging did not increase with egg volume. Consequently, within the size range observed, large and small eggs are of comparable quality. Since both the costs and benefits of large eggs compared with small eggs seem small at best, we propose that, within the size range encountered in this population, egg size can be considered an evolutionarily neutral trait.     

Genetic variation in organisms with sexual and asexual reproduction

The genetic variation in a partially asexual organism is investigated by two models suited for different time scales. Only selectively neutral variation is considered. Model 1 shows, by the use of a coalescence argument, that three sexually derived individuals per generation are sufficient to give a population the same pattern of allelic variation as found in fully sexually reproducing organisms. With less than one sexual event every third generation, the characteristic pattern expected for asexual organisms appear, with strong allelic divergence between the gene copies in individuals. At intermediary levels of sexuality, a complex situation reigns. The pair-wise allelic divergence under partial sexuality exceeds, however, always the corresponding value under full sexuality. These results apply to large populations with stable reproductive systems. In a more general framework, Model 2 shows that a small number of sexual individuals per generation is sufficient to make an apparently asexual population highly genotypically variable. The time scale in terms of generations needed to produce this effect is given by the population size and the inverse of the rate of sexuality.     

Effects of sucrose supplementation and generation on life‐history traits of Bracon cephi and Bracon lissogaster,parasitoids of the wheat stem sawfly

Knowledge of the life‐history traits that influence the reproductive success of parasitoids could provide useful information to enhance their effectiveness as biological control agents. The wheat stem sawfly Cephus cinctus Norton (Hymenoptera: Cephidae) is a major pest of wheat in the Northern Great Plains of North America. The bivoltine, sympatric and specialist parasitoids Bracon cephi (Gahan) and Bracon lissogaster Muesebeck (Hymenoptera: Braconidae) are the only species known to attack C. cinctus in wheat. In the present study, we quantify the body size, longevity, egg load and egg volume of B. cephi and B. lissogaster aiming to test whether these life‐history traits differ among adult females developing from overwintering and summer generation larvae. We also investigate the effect of sucrose supplementation on the same reproductive parameters. The results obtained show no differences between life‐history traits of B. cephi developing from the overwintering and summer generations. By contrast, the egg load of B. lissogaster is significantly different between generations, with overwintered females producing 1.2‐fold more eggs than summer individuals. Sucrose feeding has a strong positive effect on life‐history traits of both parasitoid species and generations. The longevity of sucrose‐fed females of B. cephi is increased three‐fold, whereas the survival of B. lissogaster is increased almost nine‐fold. Females of B. cephi treated with sucrose have four‐fold more mature eggs, whereas the egg load of B. lissogaster is increased 1.15‐ to 1.25‐fold with sugar feeding. Only B. cephi females increase egg volume with sucrose. The present study provides valuable insights on the life‐history and nutritional requirements of these two important parasitoid species.