Mating behavior and time budget of an androdioecious crustacean,Eulimnadia texana (Crustacea: Conchostraca)

The clam shrimp,Eulimnadia texana (Crustacea, Conchostraca), is found in freshwater ephemeral environments throughtout the United States. Individual clam shrimp of this species are either hermaphroditic or male, a relatively rare mating system for animals known as androdioecy. Comparison of sex ratios between four neighboring populations ofE. texana in Southern New Mexico showed wide variation in the ratio of males to hermaphrodites with males making up as much as 42% of some populations and not occurring at all within others. Since little is known about the behavior of this species, an ethogram and time budget were prepared based on observations of laboratory populations. Males attempt to clasp hermaphrodites prior to mating. Precopulatory mate guarding occurs in this species. Outcrossing generally occurs during mate guarding and after the hermaphrodite molts. Hermaphrodites, however, seem to control the mating process. Successful mating by males never occured if the hermaphrodite struggled with him; hermaphrodite will self in the presence of males.     

Relative fitness of two hermaphroditic mating types in the androdioecious clam shrimp,Eulimnadia texana

Androdioecy (populations of males and hermaphrodites) is a rare reproductive form, being described from only a handful of plants and animals. One of these is the shrimp Eulimnadia texana, which has populations comprised of three mating types: two hermaphroditic types (monogenics and amphigenics) and males. In a recent study, the amphigenic hermaphrodites were found to be in greater abundance than that predicted from a model of this mating system. Herein, we compare the relative fitness of offspring from amphigenic and monogenic siblings, attempting to understand the greater relative abundance of the former. Populations started with offspring from selfed monogenic hermaphrodites had a net reproductive rate (R) 87% that of offspring from their amphigenic siblings. Additionally, within populations of amphigenic offspring (which included males, monogenics and amphigenics), amphigenics survived longer than monogenics. These differences help to explain the increased relative abundance of amphigenics in natural populations, but amphigenics continue to be more abundant than expected.     

Sex chromosome evolution in the clam shrimp,Eulimnadia texana

Chromosomes that determine sex are predicted to evolve differently than autosomes: a lack of recombination on one of the two sex chromosomes is predicted to allow an accumulation of deleterious alleles that eventually leads to reduced functionality and potential physical degradation of the nonrecombining chromosome. Because these changes should occur at an elevated evolutionary rate, it is difficult to find appropriate species in which to test these evolutionary predictions. The unique genetic sex‐determining mechanism of the crustacean Eulimnadia texana prevents major chromosome degeneration because of expression of both ‘proto‐sex’ (i.e. early stage of development) chromosomes in homozygous form (ZZ and WW). Herein, we exploit this unique genetic system to examine the predicted accumulation of deleterious alleles by comparing both homogametic sexual types to their heterogametic counterpart. We report differences in crossing over in a sex‐linked region in the ZW hermaphrodites (～ 3%) relative to the ZZ males (～ 21%), indicative of cross‐over suppression in the ZW hermaphrodites. Additionally, we report that both ZZ and WW genotypes have reduced fitness relative to ZW hermaphrodites, which is consistent with the prediction of harboured recessive mutations embedded on both the Z and the W chromosomes. These results suggest that the proto‐sex chromosomes in E. texana accumulate recessive deleterious alleles. We hypothesize that recessive deleterious alleles of large effect cannot accumulate because of expression in both ZZ and WW individuals, keeping both chromosomes from losing significant function.     

Cyst development in the conchostracan shrimp,Eulimnadia texana (Crustacea: Spinicaudata)

The fertilized egg (or cyst) of branchiopods is a highly resistant stage in the life cycle of these aquatic crustaceans. Previous examinations of these cysts have determined that early embryonic development arrests at a late blastula stage, resulting in a small, crescent-shaped body within the egg shell of these shrimp. Herein, we examine the early development of these embryos by sectioning eggs in the ovotestis, brood chamber, and several time periods after exit from the brood chamber in the clam shrimp Eulimnadia texana Packard. The early sections find no evidence of internal fertilization in the ovotestis. Eggs in the ovotestis showed no signs of cell division, whereas eggs sectioned from the brood chamber were found to be undergoing early embryonic development. A number of empty egg shells and the lack of unfertilized eggs in the brood chamber suggested that egg yolks quickly degrade after egg extrusion from the ovotestis. Cysts that were allowed to develop for 24, 48, 72, and 96 h, 1 week and 1.5 years were sectioned, and embryonic development did not change after the 48 h time period. Thus, embryos appear to arrest development somewhere between 24 and 48 h after exiting the brood chamber.     

Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana

Androdioecy (mixtures of males and hermaphrodites) is a rare mating system in both plants and animals. Theory suggests that high levels of inbreeding depression can maintain males in androdioecious populations if hermaphrodites commonly self-fertilize. However, if inbreeding depression (delta) can be 'purged' from selfing populations, maintaining males is more difficult. In the androdioecious clam shrimp, Eulimnadia texana, delta is estimated to be as high as 0.7. Previous work suggests that this high level is maintained in the face of high levels of inbreeding due to an associative overdominance of fitness-related loci with the sex-determining locus. Such associative overdominance would make purging of inbreeding depression difficult to impossible. The current experiment was designed to determine if delta can be purged in these shrimp by tracking fitness across seven generations in selfing and outcrossing treatments. Evidence of purging was found in one of four populations, but the remaining populations demonstrated a consistent pattern of delta across generations. Although the experimental design allowed ample opportunity for purging, the majority of populations were unable to purge their genetic load. Therefore, delta in this species is likely due to associative overdominance caused by deleterious recessive alleles linked to the sex determining locus.     

Is sexual selection operating in the androdioecious clam shrimp,Eulimnadia texana (Crustacea: Conchostraca)?

Experiments were performed to document the existence of intersexual or intrasexual selection in the clam shrimp,Eulimnadia texana. Individuals within this species are either males or hermaphrodites. Hermaphrodites can self their own eggs or outcross with a male, but they cannot outcross with other hermaphrodites. Theoretical considerations suggest that both intrasexual and intersexual selection could be occurring on the part of the hermaphrodites and the males. When males were given a choice between two non-gravid hermaphrodites of different sizes, they did not exhibit a mating preference based upon size. When two males of different sizes were isolated with a single nongravid receptive hermaphrodite, the hermaphrodite showed no preference between the two males. There was evidence, however, of male-male competition for receptive hermaphrodites and of mate guarding on the part of the males. During aggressive encounters between twp males, the larger of the two had a significant advantage over the smaller, and larger males were always the victors hermaphrodite takeovers occurred as a result of male-male conflict. Hermaphrodites appear to control the mating process both by struglling with males when they are not receptive to them and by selfing in the presence of males. This suggests that hermaphrodites withhold receptivity cues from males, or produce non-receptivity cues, when they are going to self. Though hermaphrodites do not appear to select males based upon size, they make a selection between selfing and outcrossing by controlling the use of receptivity signals.     

A genetic comparison of two species of clam shrimp in the genus Eulimnadia: An electrophoretic approach

Herein we report the first genetic comparison among species in the genus Eulimnadia. Multilocus genotypic patterns (using six allozyme loci) were compared for a total of 2277 clam shrimp from nine populations from Arizona and New Mexico. Seven of these populations were morphologically typed as Eulimnadia texana Packard and two were typed as Eulimnadia diversa Mattox. All populations were hermaphrodite-biased, and highly inbred (inbreeding coefficients ranging from 0.33 to 0.98). Genetic distances showed the two species to be within the range described for other arthropods. One of the two E. diversa populations appeared to be a hybrid between E. texana and E. diversa, showing electrophoretic patterns similar to both species, although morphologically, they were typed as E. diversa. A phenogram (generated using coancestry distances and a neighbor joining algorithm) placed this hybrid population half-way between these two species, and a breakdown of individuals within this hybrid population (based on allozyme scores) indicated individuals very similar to the second E. diversa population, and two groups of apparent hybrid individuals. Therefore, the distinction between these two species is questionable due to their apparent hybridization in this area of Arizona. Genetic population structuring was noted among the seven E. texana pools. Estimated migration rates were less than one migrant per generation. Even in the geographically close pools in New Mexico, which were separated by only hundreds of meters, significant sub-structuring was noted, and estimates of migration rate were less than two migrants per generation.     

Notes on the life history of the clam shrimp,Eulimnadia texana

Several life history measures (growth rate, egg production, molt frequency, age at maturity and lifespan) were measured on several clam shrimp hermaphrodites (Eulimnadia texana Packard) grown in a laboratory setting under optimal growth conditions. Growth rates were high early in life, and then dropped dramatically when egg production began (day 5–6). Early egg production was low, and increased until approximately day 7, after which production leveled off for several days. Reproductive senescence was noted after day 17, with clutch sizes continuously dropping until death. Average molts per day was approximately 1.1, and molting seemed to be more closely associated with egg production than with growth. Growth and egg production were negatively correlated, indicating a possible trade-off between these two traits. No other trade-offs were detected. These shrimp show typical early-colonist life history traits, displaying high initial growth, early reproduction at a high rate, and then early senescence and death. This revised version was published online in August 2006 with corrections to the Cover Date.     

Maintenance of androdioecy in the freshwater shrimp Eulimnadia texana: sexual encounter rates and outcrossing success

The clam shrimp Eulimnadia texana has a rare mating system knownas androdioecy, in which males and hermaphrodites cooccur butthere are no pure females. In this species, reproduction takesplace by outcrossing between males and hermaphrodites, or byselfing within a hermaphrodite; this system provides a uniqueopportunity to examine the adaptive significance of out-crossingand selfing in animals. Our study examined mating behavior inhermaphrodites and males from two populations to understandthe propensity of these shrimp to mate and to estimate a parameterof a model developed by Otto et al. (American Naturalist 141:329-337),which predicts the conditions for stability of the mixed matingsystem in E. texana. Here we present evidence that mating frequencyis environmentally sensitive, with greater numbers of encountersand matings per male when males are rare and in younger males.However, the effects of shrimp density, relative male frequency,and shrimp age interact in a complex way to determine malemating success. Overall, mating frequency was determined bya combination of encounter rates between the sexes and theproportion of encounters resulting in mating. The mating rateswere then used to estimate one of four parameters of the Ottoet al. model, and these estimates were combined with previousestimates of the other three parameters to examine the fitof the predicted to the observed sex ratios in the two populations.     

Hatching conditions for Eocyzicus spinifer (Conchostraca:Crustacea) from Iraq

Some ecological aspects of Eocyzicus spinifer collected from a temporary freshwater pond near Baghdad are described. Physical and chemical variables of the pond are given. The relationship between age and growth of both sexes under laboratory conditions are documented.     

A new species of Cyzicidae (Crustacea: Conchostraca) from Iraq

A new species of Conchostraca, Eocyzicus mesopotamiensis sp. nov., from a small pond in Iraq is described and illustrated. The account includes structural details and means of recognition. Information on the habitat is also given.     

Larval and post-larval development of the branchiopod clam shrimp Cyclestheria hislopi (Baird, 1859) (Crustacea, Branchiopoda, Conchostraca, Spinicaudata)

The larval and post-larval development of Cyclestheria hislopi is examined by SEM. There are at least nine stages (excluding the adult) – six larval and three post-larval stages. The first four stages are passed within the egg-membrane. The larval and the post-larval phase are separated by a profound change in morphology that takes place between stages VI and VII. The larva shifts from a dorso-ventrally flattened 'larval' appearance up to stage VI to a laterally flattened, more 'adult' appearance from stage VII. New morphological data have been revealed by this study, including (1) a large and globular larval dorsal organ; (2) the carapace starts its development from the segments of the first and second maxillae; (3) the anterior ramus of the second antenna in adult Cyclestheria hislopi is the endopod, and the posterior ramus the exopod. Direct development of the brood in Cyclestheria hislopi – unique among conchostracans – is compared with that of the Cladocera. If Cyclestheria is the sister group to the Cladocera, as favoured in this work, the classical neoteny theory of the Cladocera must be reconsidered, as there is no particular similarity between any adults of the Cladocera and any of the larval stages of Cyclestheria . It is suggested that Cyclestheria displays the type of development present in a cladoceran ancestor. A comparison between Cyclestheria and the Upper Cambrian 'Orsten' fossil Rehbachiella kinnekullensis reveals a remarkable similarity in the endite morphology of the trunk limbs.     

Differential outcrossing rates in dispersing and non-dispersing achenes in the heterocarpic plant Crepis sancta (Asteraceae)

The association between mating systems and dispersal in plants has been studied mostly in cleistogamous species where, generally, seeds produced by cleistogamous (selfed) flowers are less dispersed than seeds produced by chasmogamous (potentially outcrossed) flowers. In heterocarpic Asteraceae, non-dispersing fruits (achenes) are produced at the periphery of the capitulum (outer florets) whereas dispersing achenes are produced by inner florets in the same capitulum. Since all the florets are protandrous, the outer floret developing first are in female phasis when anthesis of inner florets takes place. Thus, outer florets can be potentially selfed by the inner florets of the same capitulum whereas the latter must be pollinated by flowers of other capitula. Therefore outer florets should be more inbred than inner florets. To test this hypothesis, we measured the natural outcrossing rate in outer and inner florets using allozymes in three populations of the heterocarpic Crepis sancta. The results showed that the outcrossing rate was highest for non-dispersed achenes. Moreover, among the outcrossed achenes within a capitulum it was observed that the number of paternal parents of non-dispersing achenes was higher than for dispersing achenes. The pattern observed was therefore the opposite to the pattern of cleistogamous plants and contradicts the putative pollination mechanism we proposed for Asteraceae. The results agree with the predictions of sib competition theory which considers that outcrossing may minimize competitive interactions among relatives (sibs) falling near the mother plant. Higher outcrossing rate in outer florets could also occur because pollinators are more attracted to these florets.     

Selfing inNarthecium ossifragum (Melanthiaceae)

Hagerup's (1950) observations of rain pollination inNarthecium ossifragum are commonly admitted. Nevertheless,Daumann (1970) stated that pollen and stigmas suffer considerable damage from rain impact. Experimental pollinations and pollen observations were conducted at a single site in the Upper Ardennes, Belgium, during three years. Rain water had a deleterious effect on both fruit and seed set and on pollen germination. Fruit and seed set differed among years mainly due to rainy weather. Fruit set also varied among experimental treatments. Pollination trials showed thatNarthecium ossifragum is self-compatible and autofertile. Emasculation had a deleterious effect and caging had no effect on fertility.     

Methods for Inducing Selfing, Selfing and Its Role in the Life Cycle of Euplotes woodruffi syngen 3 (Ciliophora)

Methods for inducing selfing, and the relation between selfing and the life cycle of Euplotes woodruffi syngen 3 are reported. Three intercrossing stocks were used in this experiment. Selfing was induced with several treatments as follows: cell-free fluid from the cultures of complementary mating types; intact cells of GI or S phase in the cell cycle; heat-killed cells, and lysed cells of GI-, S-, and D-phase cells which were prepared by freeze-thawing. Stock SJ-27 was used as a parental stock from which Fl clones were originated through selfing. The other two stocks, SJ-8 and SJ-19, were used as testers. The period of immaturity varied from clone to clone. The heterotypic conjugation of clones with cells of stock SJ-8 seems to occur earlier in the life cycle than with cells of stock SJ-19. This result shows that this syngen has an adolescent period in the life cycle. The length of selfing immaturity seems to be different from that of crossing immaturity, and selfing appeared slightly later than crossing with testers. But the clones in which selfing 1st occurred are considered to be in adolescence or maturity, not in senility. Once selfing appeared in any clone, the clone continued to produce selfing pairs till just before clonal death. The viability of selfing and of outcrossing were compared and found not significantly different. Inbreeding depression took place in some of the F2 clones by successive selfing. The viability of F2 clones from young parents was significantly higher than that from old parents (220 to 230 fissions) both in selfing and outcrossing. The total life spans which were studied in three F1 clones were 168 to 264 fissions.     

Oviposition behavior of Edovum puttleri, reared on two hosts, Leptinotarsa decemlineata and L. texana

Female Edovum puttleri Grissell [Hymenoptera: Eulophidae], reared from eggs of Leptinotarsa decemlineata (Say) or Leptinotarsa texana Schaeffer [Coleoptera: Chrysomelidae], were videotaped as they attacked egg masses of L. decemlineata containing 20 host eggs. We identified 15 components of ovipositional behavior. Parasitoids reared on L. texana attacked and oviposited in significantly more host eggs than did females reared on L. decemlineata. Ethometric analyses of behavioral transitions and a clustering analysis of 34 behavioral parameters showed that females reared on L. texana attacked the host egg mass in a different manner than those reared from L. decemlineata. It was concluded that differences were associated with the host species upon which they were reared. Contrary to previous reports, mortality of unparasitized hosts was caused by an ovipositor probe of short duration, which was not related to host-feeding.     

Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia

Background and Aims

How and why plants evolve to become selfing is a long-standing evolutionary puzzle. The transition from outcrossing to highly selfing is less well understood in self-compatible (SC) mixed-mating (MM) species where potentially subtle interactions between floral phenotypes and the environment are at play. We examined floral morphological and developmental traits across an entire SC MM genus, Collinsia, to determine which, if any, predict potential autonomous selfing ability when pollinators are absent (AS) and actual selfing rates in the wild, s_m, and to best define the selfing syndrome for this clade.

Methods

Using polymorphic microsatellite markers, we obtained 30 population-level estimates of s_m across 19 Collinsia taxa. Species grand means for the timing of herkogamy (stigma–anther contact) and dichogamy (stigmatic receptivity, SR), AS, floral size, longevity and their genetic correlations were quantified for 22 taxa.

Key Results

Species fell into discrete selfing and outcrossing groups based on floral traits. Loss of dichogamy defines Collinsia''s selfing syndrome. Floral size, longevity and herkogamy also differ significantly between these groups. Most taxa have high AS rates (>80 %), but AS is uncorrelated with any measured trait. In contrast, s_m is significantly correlated only with SR. High variance in s_m was observed in the two groups.

Conclusions

Collinsia species exhibit clear morphological and developmental traits diagnostic of ‘selfing’ or ‘outcrossing’ groups. However, many species in both the ‘selfing’ and the ‘outcrossing’ groups were MM, pointing to the critical influence of the pollination environment, the timing of AS and outcross pollen prepotency on s_m. Flower size is a poor predictor of Collinsia species'' field selfing rates and this result may apply to many SC species. Assessment of the variation in the pollination environment, which can increase selfing rates in more ‘outcrossing’ species but can also decrease selfing rates in more ‘selfing’ species, is critical to understanding mating system evolution of SC MM taxa.     

Early Developmental Stages of the Green Tiger Prawn, Penaeus semisulcatus de Haan (Crustacea, Decapoda, Penaeidae)

Gravid females of Penaeus semisulcatus were spawned in the laboratory by natural means. The embryos were documented and the larvae were reared from hatching to postlarval stage at 28.2–30.0 °C and 33.5–34.5 g kg⁻¹ salinity for about 10 days (223 h 55 min). Six naupliar stages, three protozoea stages, three mysis stages and the first postlarval stage were described and illustrated. The larvae were fed only with microalgae Tetraselmis tetrathele and Chaetoceros gracilis from first protozoea until the second mysis, with about 90% survival rate; from the third mysis until the first postlarva they were fed with similar microalgae coupled with rotifer Brachionus plicatilis and Artemia nauplii. The embryonic and larval stages of P. semisulcatus are generally similar to those of other closely related species in the family Penaeidae, such as Melicertus canaliculatus, Fenneropenaeus merguiensis, and Marsupenaeus japonicus, except for the size and structure of diagnostic characters, setation of appendages and duration of metamorphoses. The change in the feeding habit during ontogeny was related to morphological transformation of the feeding apparatus of larvae and postlarvae. This paper is the first comprehensive and complete account of the early developmental stages of P. semisulcatus.     

Uptake of lead,cadmium and zinc by the fairy shrimp,Branchinecta longiantenna (Crustacea: Anostraca)

Individuals of the fairy shrimp, Branchinecta longiantenna, were subjected to 5 concentrations (0.1 to 15 mg l^–1) of Pb in diluted habitat water at 13 °C. Lead concentrations (mg kg^–1 wet weight) in the animals were determined at 2-day intervals by digestion in nitric acid followed by atomic absorption analysis. The shrimp were also subjected to 0.1 mg l^–1 media of Cd and Zn, separately.Uptake rates by the fairy shrimp for the three metal ions at 0.1 mg l^–1 were: 0.111, 0.0885, and 0.0460 mg kg^–1 day^–1 for Zn, Pb, and Cd, respectively. After 2 days in 1.0 mg l^–1 Cd or Zn, the animals expired; but they surviced for 8 days in a 10 mg l^–1 Pb medium and for 2 days in 25 mg l^–1 Pb. Lead uptake demonstrated a linear dependence on the Pb concentration in the media.Shrimp survived at much higher tissue accumulations of Pb compared to Zn and Cd. Estimated lethal doses were 20, 1.2–2.4, and 0.4–1.4 mg kg^–1 wet weight for Pb, Zn, and Cd, respectively. Pb was found to be at much lower concentration than Cd or Zn in the natural pond water but between Cd and Zn levels in the sediment. Thus Cd and Zn probably present a greater threat to B. longiantenna than Pb, although Pb may be in higher concentration in the environment.Contribution 47, Laboratory of Ecology, The Claremont Colleges, Claremont, CA 91711, USA. Send reprint requests to Clyde Eriksen.     

New hyalellids (Crustacea, Amphipoda, Hyalellidae) from Lake Titicaca

Two new species of hyalellid amphipods, Hyalella crawfordi and H. gauthieri, are described from Lake Titicaca; H. echinus (Faxon, 1876) is redescribed. The H. echinus group of species is newly proposed for these three species, and a group diagnosis is provided. A key to the three species in the group is provided Full article published online at http://www.senckenberg.de/odes/06-10.htm.