Potential for parthenogenesis of virgin females in a bisexual population of the geographically parthenogenetic mayfly Ephoron shigae (Insecta: Ephemeroptera,Polymitarcyidae)

The burrowing polymitarcyid mayfly Ephoron shigae is a geographically parthenogenetic species. Interestingly, the distributions of the bisexual and unisexual populations overlap broadly in their respective geographic ranges. In this mayfly, obligatory diploid thelytoky appears within unisexual populations. In the present study, we examined the potential for parthenogenesis or the parthenogenetic ability of females in a bisexual population aiming to understand the emergence of unisexual populations. The results obtained revealed that females in the examined bisexual populations showed a potential for diploid thelytoky as also seen in the unisexual populations, although, in females from bisexual populations, the development success rates of their unfertilized eggs were considerably lower than those of virgin females from unisexual populations. In the three bisexual reproducing species (Ephemera japonica, Ephemera strigata, and Ephemera orientalis) in the closely‐related family Ephemeridae, diploid thelytoky (i.e. tychoparthenogenesis; < 3%) was also observed. However, in this case, the parthenogenetic development success rates of unfertilized eggs were significantly lower than those of virgin females in the bisexual (Hino‐yosui Irrigation Canal) population of E. shigae. Accordingly, we suggest that parthenogenetic ability (i.e. tychoparthenogenesis or facultative parthenogenesis) in bisexual populations of E. shigae may facilitate the evolutionary transition to unisexual populations with fully obligatory parthenogenesis. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 326–334.     

Geographical variation in Japan in egg development of the mayfly, Ephoron shigae (Ephemeroptera: Polymitarcyidae)

1. The effect of temperature on embryonic development was compared in four populations, two bisexual and two unisexual, of Ephoron shigae , including one each near the northern and southern periphery of the species range in Japan.
2. Eggs from every population were chilled at 4, 8 or 12 °C for diapause development after 50 days at 20 °C for pre-diapause development (experiment I). Some eggs hatched during chilling at 8 °C or 12 °C, whereas no eggs hatched at 4 °C. The rate of hatching in a given condition of chilling was higher for the eggs from warmer winter environments.
3. Chilling at 4 or 8 °C effectively facilitated diapause development. Chilling at 12 °C was, in general, not so effective, but relatively effective for the eggs from warmer winter environments.
4. Eggs were incubated at 8, 12, 15 or 20 °C after chilling at 4 °C to examine the effect of temperature on post-diapause development (experiment II). The eggs incubated at higher temperature after chilling hatched quicker and more synchronously and had higher hatching success.
5. The relationship between temperature and the days required for hatching after chilling was well described by the power function. There was no significant difference in the slope of the regression lines (i.e. temperature dependency) among local populations. However, a longer time was required for hatching at a given temperature for the population from the colder winter environment.
6. There was no detectable difference in the observed intraspecific variations between unisexual and bisexual populations.     

Reproductive mode of the geographic parthenogenetic mayfly Ephoron shigae, with findings from some new localities (Insecta: Ephemeroptera, Polymitarcyidae)

The burrowing polymitarcyid mayfly Ephoron shigae is distributed widely in Japan. Some populations are bisexual, others are unisexual, and the distributions of the two types overlap broadly. Experimental evidence of parthenogenetic reproduction, long suspected in unisexual populations, is presented here, based on a comparative analysis of the developmental rate of fertilized and unfertilized eggs. The developmental rate of fertilized eggs from 20 mated females in a bisexual population was 98.4% ± 0.73% (mean ± SD), and no unfertilized eggs from 20 virgin females in that population developed. The developmental rates of unfertilized eggs in two unisexual populations were 89.0% ± 4.59% and 84.2% ± 1.96%, respectively. This article presents experimental evidence of geographic parthenogenesis in E. shigae and provides support for the previous interpretation. In addition, we discuss the relationship between the sex ratio of each population and the developmental rate of fertilized versus unfertilized eggs from the females in those populations.     

Phylogenetic relationships among bisexual and unisexual lineages of the weevil Scepticus insularis (Coleoptera: Curculionidae) on Hokkaido, Northern Japan

We examined the geographic distributions and phylogenetic relationships of bisexual and unisexual (parthenogenetic) forms of the weevil Scepticus insularis on Hokkaido Island, northern Japan. Unisexual beetles were widespread throughout Hokkaido, whereas bisexuals were found only in three remote areas. Bisexuals (females and males) and unisexual females occurred sympatrically in two areas. We determined nucleotide sequences for part of the mitochondrial NADH dehydrogenase subunit 2 (ND2; 633 bp) gene for 104 individuals, and for part of the nuclear internal transcribed spacer region 2 (ITS2; 360 bp) for 91 individuals. In an ND2 gene tree, haplotypes of S. insularis fell into two distinct clades (A and B), which were genetically differentiated from one another by 9.1% nucleotide sequence divergence. Haplotypes of females identified as unisexual were all in clade A, whereas those of females identified as bisexual belonged to clade B. Haplotypes of males were in clade B, except for two males having a clade-A haplotype. Circumstantial evidence suggests that these two males were produced by unisexual females. The ND2 tree suggests that the current unisexual form of S. insularis on Hokkaido was of a single origin. In contrast, a gene tree for ITS2 haplotypes show no clear divergence between the two modes of reproduction, with two major haplotypes shared by unisexual females, bisexual females, and males. This incongruence between the nuclear and mitochondrial phylogenies may be attributable to occasional gene flow between the unisexual and bisexual lineages through males occasionally produced by unisexual females, but our results do not exclude the possibility that the two lineages share polymorphic ancestral ITS2 haplotypes.     

Interspecific and intraspecific variations in egg hatching for British populations of the stoneflies Siphonoperla torrentium and Chloroperia tripunctata (Plecoptera: Chloroperiidae)

SUMMARY 1. The objective was to compare variations in egg hatching between the two species (interspecific variations) and between populations of the same species (intraspecific variations). There were significant interspecific, but not intraspecific, differences in female size, adult life-span, egg production, hatching success, incubation periods and hatching periods.
2. The optimum temperature for hatching success within the range 3.8–22.1°C in the laboratory and the range over which at least 50% of the eggs hatched were lower for Chloroperia tripunctata (Scopoli) (8.5°C, 4.2–17.3°C) than for Siphonoperla torrentium (Pictet) (12.8°C, 6.1–19.4°C). Few eggs hatched at 22.r°C.
3. The relationship between incubation period (d days) and water temperature (T°C) was given by: d=1219/T^1.368 for S. torrentium , d=253/T^0.459 for C. tripunctata . Both equations successfully predicted incubation periods for eggs placed in a stream. The period over which eggs hatched was much longer for C. tripunctata than for S. torrentium at all temperatures.
4. The shorter incubation period (at r>5.6°C) and shorter hatching period for S. torrentium ensure that larvae of this species are already growing when eggs of C. tripunctata start to hatch, but the prolonged hatching period of the latter species ensures a long period of larval recruitment to the population. These differences in egg hatching may reduce competition between the two closely-related species.     

Reproductive isolation and genetic differentiation in North American species of Triops (Crustacea: Branchiopoda: Notostraca)

Electrophoretic analysis of 31 populations, ranging from California to Kansas, indicates that the North American tadpole shrimp Triops longicaudatus (LeConte) is actually a mixture of at least two reproductively isolated species. In the central United States, the predominant species is T. longicaudatus, which is found typically in ephemeral prairie pools. In the southwestern United States, the predominant species is Triops newberryi (Packard), which characteristically inhabits large playa pools. The two species coexist occasionally and in sympatric situations they are reproductively isolated from each other. The two species are genetically distinct at a level greater than is typical of conspecific populations. These genetic differences are correlated with subtle morphological differences and profound differences in reproductive biology. Both species represent complexes of bisexual and unisexual populations. Bisexual populations of T. longicaudatus are usually composed of males and females in approximately equal frequencies; bisexual populations of T. newberryi are composed of males in low frequencies and self-compatible hermaphrodites. Unisexual populations of both species apparently consist entirely of self-compatible hermaphrodites. This revised version was published online in August 2006 with corrections to the Cover Date.     

ANDROGENETICS AND TRIPLOIDS FROM AN INTERACTING PARTHENOGENETIC HYBRID AND ITS ANCESTORS IN STICK INSECTS

Populations of unisexual organisms are often assumed to be genetically invariant (clones) and destined to a short existence on an evolutionary timescale. Unisexual organisms are most often obligate parthenogens and, by definition, ought to be completely isolated reproductively from related bisexual organisms. The assumption of complete reproductive isolation between amphimictic ancestors and thelytokous hybrids is common to most hypotheses on the evolution of sex and its adaptive significance. Stick insects of the genus Bacillus however provide evidence for reproductive interactions between allodiploid parthenogens and their ancestors, because pure species progeny (androgenetics) and triploid descendants are produced. These findings demonstrate that, through androgenesis, offspring of parthenogenetic hybrid females can contribute specimens of both sexes to the fathering species when fertilized by syntopic ancestral males and the parthenogenetic egg of strictly clonal females, when fertilized, allows a third genome to be added to the allodiploid chromosome set. These triploid genomes promote further genetic diversification and evolution of the unisexual populations through the formation of new clones by recombination during the changed maturation mode of allotriploid eggs. All this argues for much more complex breeding systems and evolutionary pathways than are usually assumed for hybrid unisexual organisms.     

Interspecific and intraspecific variations in egg hatching for British populations of Taeniopteryx nebulosa and Brachyptera risi (Plecoptera: Taeniopterygidae)

Adults were obtained from three populations of Taeniopteryx nebulosa and four populations of Brachyptera risi ; their eggs were incubated at seven constant temperatures (range 3.8–22.1°C). There were interspecific, but not intraspecific, differences in adult life-span, mean number of eggs laid per female, hatching success and egg incubation periods. The optimum temperature for hatching success and the range over which at least 50% of the eggs hatched were lower for T. nebulosa (6.5°C, 2.7–15.0°C) than for B. risi (9.0°C, 5.1–15.8°C). No eggs hatched at 22.1°C. The relationship between incubation period (d days) and water temperature (T°C) was given by; d = 326.4 T^−1.015 for T. nebulosa , d = 824.0 T^−0.739 for B. risi . Both equations successfully predicted incubation periods for eggs placed in a stream.
Hatching success and incubation periods were similar to those already published for a Norwegian population of T. nebulosa . The lack of significant intraspecific variation suggests that the genotypes associated with the variables examined in this study have remained remarkably stable in these two species in spite of the geographical isolation of their different populations.     

THE EVOLUTIONARY HISTORY OF PARTHENOGENETIC CNEMIDOPHORUS LEMNISCATUS (SAURIA: TEIIDAE). II. MATERNAL ORIGIN AND AGE INFERRED FROM MITOCHONDRIAL DNA ANALYSES

Restriction endonuclease analyses were performed on mitochondrial DNAs (mtDNAs) representing unisexual parthenogenetic (cytotypes A, B, and C) and bisexual (cytotypes D and E) populations of Amazonian lizards presently regarded as Cnemidophorus lemniscatus. The results of mtDNA cleavage map comparisons among these C. lemniscatus indicated that (1) there was no cleavage site variation among the unisexuals, (2) mtDNAs from the bisexual cytotypes D and E differed in sequence from one another by about 13%, and (3) mtDNAs from cytotypes A–C differed from those of cytotype D by about 5% and from those of cytotype E by about 13%. Higher resolution restriction fragment size comparisons confirmed the high degree of similarity among the unisexual mtDNAs, but identified 12 cleavage site variants among the 13 cytotype D mtDNAs examined. Both cladistic and phenetic (UPGMA) analyses of the data indicate that the unisexual and cytotype D mtDNAs form a single clade, suggesting that a female of cytotype D was the maternal progenitor of the unisexuals. The similarity among the unisexual mtDNAs and the variability among those of cytotype D suggest that the three unisexual cytotypes arose recently from a common maternal lineage. The mtDNA variability observed among cytotype D individuals has a strong geographic component, suggesting that the unisexuals arose from one or a few geographically proximal populations. The mtDNA comparisons also support the conclusion, based on allozyme comparisons (Sites et al., 1990, this issue), that cytotypes D and E, although presently allocated to C. lemniscatus, are separate species.     

Temperature-dependent development rates of cod Gadus morhua eggs

Temperature development relationships were determined for batches of Irish Sea cod Gadus morhua eggs incubated in flow-through incubators. Hatching began 16·4 days after fertilization (DAF) at 6° C, 10·3 DAF at 8° C, 9·4 DAF at 10° C and 7·4 DAF at 12° C. Egg mortality increased at the higher temperatures, but survival was >80%. Results were compared with published data at four comparable stage end points: the end of blastula, the end of gastrula, the point of growth of the embryo completely surrounding the yolk and the point when 50% of the eggs were hatched. All the studies showed a curvilinear relationship between age at stage and temperature. There was a 12 day inter-study difference in time to 50% hatch at 2° C and 4 day difference at 10° C. There were no consistent trends that differentiated eastern v. western, or northern v. southern populations. A single model for cod egg incubation time from fertilization to 50% hatch was derived based on data from six cod populations, but it is recommended that individual stock relationships should be used where possible.     

Synchronization of larval emergence in winter moth (Operophtera brumata L.) and budburst in pedunculate oak (Quercus robur L.) under simulated climate change

1. The hypothesis that a 3 °C elevation in temperature and doubled CO₂ concentration would have no effect on the synchronization of winter moth egg hatch with budburst in oak was tested by comparing the separate and interactive effects of ambient and elevated (+ 3 °C) temperature and ambient and elevated (doubled to 340 p.p.m.) CO₂ in eight experimental Solardomes. In addition, an outdoor control was compared with the ambient temperature/CO₂ treatment combination.
2. Elevated temperature accelerated darkening (preceding egg hatch by about 5–10 days) and hatching of eggs developing off the trees; elevated CO₂ had no effect. The same effects were observed in eggs developing on the trees.
3. Within treatments, date of egg hatch was the same on trees with early or late budburst.
4. Egg darkening and budburst were closely synchronized at both ambient and elevated temperatures.
5. Both eggs and trees required fewer cumulative heat units (day degrees > 4 °C), for hatching and budburst, respectively, at ambient than elevated temperatures. The requirements in the outdoor control treatment were similar to those in the ambient Solardome treatment.
6. Egg hatch between 10 and 25 °C, on a temperature gradient in the laboratory, required a constant number of heat units; fewer were required below 10 °C.
7. Elevated temperatures, in the Solardomes and the field, delayed adult emergence from the pupae.
8. The results suggest that a general increase in temperature with climatic change would not affect the closeness of the synchronization between egg hatch of winter moth and budburst of oak.     

UNISEXUAL/BISEXUAL BREEDING COMPLEXES IN POECILIIDAE: WHY DO MALES COPULATE WITH UNISEXUAL FEMALES?

Unisexual poeciliid fishes live as sexual parasites in breeding complexes with related bisexual species. Males of the host species copulate with unisexual females as well as with con-specifics, thus maintaining the unisexuals. Copulation with a unisexual offers no selective benefit for a male. A model is proposed that provides an explanation in terms of evolutionary ecology for why males copulate with unisexuals. It assumes that, before copulation, a male attempts to identify a female as conspecific or not but that the correctness of the identification depends on the length of time spent on the identification process. Some cost is involved in the passage of time, so an optimal time spent on identification must exist. Because subordinate males risk being driven away by dominant males, the optimal time is longer for males at the top of the dominance hierarchy than for males at the bottom. Such an optimal strategy gives a male the greatest possible average net benefit from a mating attempt, given his social status; this is a “best of a bad job” strategy.     

Population variation and ecological correlates of tychoparthenogenesis in the mayfly, Stenonema femoratum

Species in which both sex and parthenogenesis co‐occur are extremely valuable for investigating ecological conditions favouring sex. Tychoparthenogenesis is a breeding system characterized by hatching of a small proportion of unfertilized eggs (typically < 10%) from females of sexually reproducing species. With tychoparthenogenesis, both sexual and parthenogenetic reproduction co‐occur within the same population. To identify ecological conditions that may favour this breeding system, I quantified population variation in females’ capacity for tychoparthenogenesis and investigated biotic and abiotic correlates of tychoparthenogenesis. I estimated tychoparthenognetic capacity (proportion of unfertilized eggs hatching) for females from 12 Missouri populations of the mayfly, Stenonema femoratum (Ephemeroptera: Heptageniidae), across three different habitat types – temporary streams, permanent streams and lakes. Tychoparthenogenetic capacity, measured as the population mean hatch success of unfertilized eggs, ranged from 3.8 to 10.7%. Tychoparthenogenetic capacity varied among habitats in 1996, but not in 1997. In 1996, temporary streams showed hatch success of unfertilized eggs twice that of permanent streams and lakes. Tychoparthenogenetic capacity also varied among sampling dates within years. Temporary streams also showed extremely low nymph densities compared to the other two habitats. However, habitats did not differ in adult density. Furthermore, in all populations nymphs showed significantly female‐biased sex ratios. In contrast, adult sex ratios were equal or slightly male biased. Tychoparthenogenetic capacity was negatively correlated with nymph density in 1996, but not in 1997, suggesting possible reproductive assurance in some years. Adult densities also suggested that there may be certain times of year when tychoparthenogenesis may provide benefits of reproductive assurance. Although habitats differed significantly in their abiotic characteristics, tychoparthenogenetic capacity was correlated significantly with water temperature only. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75 , 101–123.     

Intra- and inter-specific variations in egg survival and brood development time for Austrian populations of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda)

SUMMARY. 1. Egg survival (ES, percentage of eggs hatched in vitro ), reproductive success (RS, percentage of live young released from the brood pouch) and brood development lime ( d , days) in four populations of Gammarus fossarum and two populations of Gammarus roeseli were studied, in the laboratory at water temperatures of 2.0–26.1°C. Intraspecific differences between populations were not significant, but interspecific differences were found between the two species.
2. In natural stream populations, the reproductive period of G. fossarum lasted from December to September, that of G. roeseli from March to September.
3. In the experimental temperature range 2–26°C, 73% of the total number (771) of G. fossarum females and 69% of 469 G. roeseli females were ovigerous. Of these, 45% of G. fossarum and 43% of G. roeseli females successfully released live young from their brood pouches.
4. For G. fossarum , the optimum temperatures were 11.4°C for ES, where 76% of the eggs hatched, and 11.8°C for RS, where 77% of the females released live young from their brood pouches. For G. roseli , the optimum temperatures were 13.5°C for ES (51% hatched) and 14.0°C for RS (76% released). Over 50% of eggs hatched at temperatures of 3.6–19.2°C in G. fossarum and at 1 1.9–15.1°C in G. roeseli . Development time increased from 12 days at 21.9°C to 251 days at 2.0°C in G. fossarum , and from 10 days at 24.1°C to 212 days at 4.1°C in G. roeseli .
5. interspecific differences between the effects of water temperature on ES, RS and d are used to explain the different distributional patterns of G. fossarum and G. roeseli in central European running water systems. assuming that other physico-chemical variables are suitable for both species.     

Aspects of the mating behaviour of male mollies (Poecilia spp.)

The unisexual fish Poecilia formosa (the Amazon molly) reproduces by gynogenesis, a process in which sperm from the males of the host bisexual species activates development of its eggs. Unisexuals live with one of the host species in nature and compete with bisexual females for the males. It was long thought that male discrimination and mate selection established a balance between the unisexual and bisexual populations. Thus, hierarchies of males were set up in which dominant males mated with their conspecific females and subordinates mated with the Amazon molly. Recent evidence suggested, however, that male fish do not discriminate between their own females and the Amazon molly, and that there always are more males available than sexually receptive females of both species.
Our findings indicate that male behaviour may be more complex than suggested by either hypothesis. Mate discrimination and courtship behaviour appear to increase with age, so that large males show almost complete preference for their conspecific females, but smaller males will mate with the Amazon molly. In complex groups, small males often dart in and mate with their own females whilst the large males are engaged in courtship activities and defence of territory.     

Parthenogenesis in the Two Races of Radopholus similis from Florida

Single larval inoculations of both the citrus and banana races of Radopholus similis from Florida indicate parthenogenetic reproduction is possible. These races normally reproduce amphimictieally. Both races produced all-female populations from single larva inoculations after 80 d and male-female populations after 180 d. The all-female populations produced female progeny with viable eggs, but no spermatozoa were present in the spermatheca, indicating tychoparthenogenesis occurred. Uninseminated females in the latter study produced both male and female progeny. Approximately 95% of the female progeny of the male-female populations were inseminated, indicating that cross-fertilization had occurred. The proportion of males to females was as expected in a normal bisexual population. No intersex males were observed. The mechanism of sex determination is not fully understood but assumed to be enviromnentally induced.     

Incubation of eggs of tuatara, Sphenodon punctatus

Eggs of the tuatara, Sphenodon punctatus , were incubated either buried or half buried in vermiculite at constant temperatures of 15, 18, 20, 22 and 25 °C and constant water potentials between —90 and —400 kPa. Many clutches failed completely, possibly because they had been taken from females prior to proper shell development. Failed eggs were significantly smaller than successful eggs. Incubation is unsuccessful at 15 °C. Hatching success is high between 18 and 22 °C but low at 25 °C, but equally successful between 18 and 22°C. Incubation is strongly influenced by temperature, with mean incubation periods of 328 days at 18 °C, 259 days at 20 °C, 169 days at 22 °C and 150 days at 25 °C. Water potential generally has little influence on incubation time at a given temperature. Buried eggs hatch sooner than partially buried eggs at 20 °C but the large range makes significance dubious.
Eggs on the driest substrata at 18 and 20 °C lose water initially but then gain water through the rest of incubation. Eggs in all other conditions gain water throughout incubation, with the rate of i water absorption being maintained or increasing late in incubation. The suggestion that increasing rate of water absorption late in incubation facilitates explosive hatching is not supported. Egg mass at the time of hatching varies from 132 to 398% of initial values, depending on incubation conditions. Final egg mass is not affected significantly by incubation temperature. Hence, rates of absorption increase with temperature.
Water potential has no influence on hatchling size. However, hatchlings from buried eggs generally are significantly larger than those from partially buried eggs.     

The question of paternal investment in Lepidoptera: male-contributed proteins in Plodia interpunctella

In Plodia interpunctella, radioactive labelling techniques indicate that male-derived substances, transferred to the female during copulation, enter unfertilized eggs. These substances are proteinaceous and the cumulative amount of material entering the unfertilized eggs increases with time since mating. Following courtship, smaller males complete coupling with females at a lower frequency than larger males. Smaller males also transfer smaller (by weight) ejaculates than larger males. Ejaculate weight is about 4% of male body weight in P. interpunctella. However, neither fecundity nor the number of deposited eggs are a function of ejaculate weight. Consequently, ejaculate materials cannot be designated a form of paternal investment, despite the observed transfer to unfertilized eggs.     

The prevalence of genome replacement in unisexual salamanders of the genus <Emphasis Type="Italic">Ambystoma</Emphasis>(Amphibia,Caudata) revealed by nuclear gene genealogy

Background  

Unisexual salamanders of the genus Ambystoma exemplify the most ancient lineage of unisexual vertebrates and demonstrate an extremely flexible reproductive system. Unisexual Ambystoma interact with and incorporate genomes from two to four sexual species (A. laterale, A. jeffersonianum, A. texanum, and A. tigrinum), to generate more than 20 genome compositions or biotypes. Unisexual ploidy levels range from diploid to pentaploid, but all contain at least one A. laterale (L) genome. Replacement of nuclear genomes might be responsible for the evolutionary longevity of unisexual Ambystoma but direct evidence for the prevalence of genome replacement in natural populations is absent. Two major puzzling questions have remained unanswered over the last few decades: 1) is genome replacement a common reproductive method in various unisexual populations and, 2) is there an ancient "L" genome that persists in various unisexual genome compositions.