The detection of new rickettsial and coccidian infections in the ovary and further organs raises fears that the marbled crayfish might endanger native European species by transmission of pathogens once escaped into the wild. Volume , Issue 3. If you do not receive an email within 10 minutes, your email address may not be registered, and you may need to create a new Wiley Online Library account.
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Journal of Morphology Volume , Issue 3. Tools Request permission Export citation Add to favorites Track citation. Share Give access Share full text access. Share full text access. Please review our Terms and Conditions of Use and check box below to share full-text version of article. Abstract Recently, we briefly reported on the first case of parthenogenesis in the decapod Crustacea which was found in the Marmorkrebs or marbled crayfish, a cambarid species of unknown geographic origin and species identity. Citing Literature.
Volume , Issue 3 September Pages Related Information. Close Figure Viewer. Browse All Figures Return to Figure. Previous Figure Next Figure. Email or Customer ID. Forgot password? Old Password. We provide experimental evidence that females of one cambarid species particularly widespread in Europe, the spiny-cheek crayfish Orconectes limosus , are capable of facultative parthenogenesis. Such reproductive mode has never before been recognized in decapods, the most diverse crustacean order.
As shown by analysis of seven microsatellite loci, crayfish females kept physically separated from males produced genetically homogeneous offspring identical with maternal individuals; this suggests they reproduced by apomixis, unlike those females which mated with males and had a diverse offspring. Further research is needed to clarify what environmental conditions are necessary for a switch to parthenogenesis in O. However, if such reproductive plasticity is present in other cambarid crayfish species, it may contribute to the overwhelming invasive success of this group.
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.
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Crayfish are ecologically important benthic macroinvertebrates, and often act as keystone species in both standing and running waters . Since they are also economically important, many crayfish species have been introduced to regions outside of their original distributions, both within and between continents.
Reproductive Biology of Crustaceans | Case Studies of Decapod Crustaceans | Taylor & Francis Group
The introduction of North American crayfish to Europe has been particularly successful, but has also had serious conservational consequences, including the decimation of local crayfish populations by the crayfish plague pathogen introduced with them . The first of those species, the spiny-cheek crayfish Orconectes limosus Figure 1 , became successfully established from a batch of 90 individuals released in to a fishpond in Pomerania presently western Poland , and has since colonized at least 20 European countries  , . Other American crayfish have since been introduced to Europe, resulting in at least eight to nine species established at present  , .
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There was no difference in phenotype of females in the different experimental groups. Recently, the obligate asexual marbled crayfish, later shown to be a parthenogenetic form of Procambarus fallax  , was discovered in the aquarium trade .
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Since then, it has been released to open waters and become established at several localities  ,  ; however, asexually reproducing crayfish are not known from the original distribution of the species. Marbled crayfish, so far the only known parthenogenetic decapod crustacean, which completely lacks males, is considered to be a serious future threat to aquatic biodiversity in regions where it becomes established  ,  , although its success in European waters seems to be constrained by climate . No other crayfish or any other decapod crustacean proven to be capable of asexual reproduction is known from the wild.
All except one of the American crayfish invaders belong to the family Cambaridae, and their life histories are typical for r-strategists. Unlike native European astacid crayfish, many cambarids living in temperate climates, including O. The adaptive value of this feature of their life cycle is unknown. In order to explore the impact of different mating patterns and the availability of mates to the reproductive success of O. For this purpose, we distributed the animals into three experimental groups. Two groups consisted of thirty females and fifteen males, which were allowed visual, chemical, and tactile contact, including mating behaviour.
Thus, the two sexes were denied the physical contact but chemical communication was allowed. Females in this group were physically isolated from males for ten months; despite that, vast majority of them successfully spawned and carried clutches of apparently viable offspring. We provide evidence that the species is capable of facultative parthenogenesis, a reproductive mode not reported before in decapod crustaceans.
Two of these females later lost the eggs, but the remaining 26 individuals reared viable offspring that developed normally until the 3 rd developmental stage when the juveniles become independent. In these, 27 and 25 females spawned, and subsequently 25 and 20 individuals reared viable offspring. Subsequent analysis of seven variable microsatellite loci  for 23 females and 10 juveniles from each of their broods showed that all analysed offspring produced in the absence of males had multilocus genotypes identical to their mothers, which were often heterozygous at several—up to all seven—loci their multilocus genotypes are given in Table S1.
Females mated to males produced genetically diverse offspring; none of the analysed juveniles had a multilocus genotype identical to its mother, and they often carried alleles not observed in the maternal individual, i. The observation that females prevented from physical contact with males for ten months successfully spawned and reared viable offspring was intriguing. Such a phenomenon could be explained by several different scenarios, most of which assume that the eggs produced by females were somehow fertilized despite physical isolation from males.
At first glance, the most feasible explanation is long-term storage of sperm in the annulus ventralis of females, as documented in another cambarid species . Although the females were kept in isolation from males for ten months beginning in August, so mating would have had to occur even earlier in the previous season, a sperm retention seemed still more likely than other possible explanations. The fact that males and females, though physically separated by a mesh and a water column, shared the same container, allows for speculation about some mechanism of sperm transfer, although such external fertilization is not known for crayfish.
Reproductive Biology of Crustaceans
Alternatively, sexual reproduction might have occurred if some individuals exhibiting a female phenotype had functional male gonads. Although intersex and gynandromorph individuals have been recorded in various crayfish taxa  ,  and hermaphroditism seems to be common in some parastacid crayfish from the Southern Hemisphere  ,  , none of the females selected for our experiment had any aberration in their first pleopods or other sex-related phenotypic characters.
All above-mentioned scenarios have in common the fact that they assume sexual reproduction; the produced offspring would therefore be genetically diverse, and at least some juveniles would carry paternal alleles not found in their mother. Finally, females that could not mate with males could have resorted to parthenogenetic reproduction. This scenario predicts that the offspring carry only maternal alleles; depending on the type of parthenogenesis, all juveniles might be identical to their mothers in the case of apomixis  or the maternal alleles might be recombined in the juveniles in the case of automixis, in which meiosis is not suppressed  , .
Automixis should also result in loss of heterozygosity of the parthenogenetic offspring  , . In contrast, mated females produced genetically diverse offspring as expected in sexually reproducing specimens. These results strongly suggest that O. Facultative parthenogenesis is not a particularly rare phenomenon in animals.
Clonal and sexual reproduction regularly alternates in some invertebrate groups e. In captivity, it has been documented for various vertebrates  , even in such charismatic species such as the hammerhead shark  and the Komodo dragon . Nevertheless, this mode of reproduction has, to our knowledge, never been observed in decapod crustaceans, the most diverse and economically most important crustacean order. Apart from the marbled crayfish obligately reproducing by apomictic parthenogenesis  , the only other decapod species for which a potential for asexual reproduction has been suggested based on the observation of various individuals with identical five-microsatellite multilocus genotypes is the red swamp crayfish Procambarus clarkii .
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In the latter case, the observed genotype identities of some wild-caught crayfish could also be explained by other processes in particular, chance sampling of sibling individuals from the same brood. However, Yue et al. A major question remains why facultative asexuality has not previously been reported for the spiny-cheek crayfish, a species that has been present in Europe for more than a century and has been the subject of numerous studies.
Most likely, parthenogenetic reproduction may be triggered only under special circumstances, when males are unavailable for mating. Females mated to males in our experiment had significantly larger clutch sizes than those reproducing parthenogenetically; this suggests some costs to asexuality.
The role of different factors remains to be explored by further experimental work; however, we suggest several that may play a role in switching between alternative reproductive strategies. First, if infochemicals released from males during the mating season indicate the presence of the opposite sex but mating is not possible due to physical isolation, females not finding mates during the suitable period despite sensing their presence may resort to parthenogenesis rather than skipping one reproductive season entirely.
Last but not least, adequate abiotic conditions such as light and temperature regimes corresponding to the mating season may also be necessary for triggering parthenogenesis in both natural and artificial conditions. It is possible that a combination of several different factors is required for a successful switch to asexual reproduction, which limits the likelihood that the phenomenon occurs in laboratory cultures. Nevertheless, we had already previously observed the spawning of O.
At that time, however, we did not further examine these females or their broods. The fact that this phenomenon was initially overlooked even by our group focused on crayfish biology brings up another likely explanation for the lack of data on parthenogenetic reproduction in cambarid crayfish: earlier casual observers of facultative parthenogenesis may have just dismissed the observation as an experimental artefact in particular, a previously undetected mating.
It has generally been stated that crayfish do not reproduce asexually, so any case when apparently unmated females released eggs would likely have been attributed to sperm storage in the annulus ventralis , which had been documented earlier . Similarly, indirect evidence of the potential contribution of asexual reproduction to the genetic structure of natural populations, such as Hardy-Weinberg disequilibrium, may have other more feasible explanations the Wahlund effect, the presence of null alleles, assortative mating, etc.
Our experiment, complemented by the genetic analysis of variable nuclear markers, proves that at least one species of cambarid crayfish is capable of facultative parthenogenesis. The actual prevalence of this phenomenon under natural conditions is not known. However, it is possible that this reproductive mode is more widespread among cambarids, and contributes to the success of this group when colonizing new habitats and territories.
Asexual reproduction might also have contributed to observations of putative P. However, despite the apparent ability of O. Apparently, sexual reproduction in this species strongly dominates, or is the only reproduction mode in established populations where males are present. It remains to be tested whether females of this species are able to reproduce entirely without males; so far, there has been no report of female-only populations of any cambarid with the exception of established marbled crayfish populations, for which asexuality is the sole reproduction mode  , .
The fact that unmated spiny-cheek crayfish females produced a significantly lower number of eggs is notable. It is possible that although less numerous, clonally-produced eggs are larger than those from mated females; such adjustments in female primary reproductive investment have been reported in crayfish .
Alternatively, clonal offspring could be less fit, e. Facultative parthenogenetic reproduction might have also promoted the evolution of the prolonged or double mating season in cambarids. This life history trait could increase the likelihood of females finding mates before resorting to asexual reproduction as an alternative strategy that leads to lower offspring numbers; double mating may also serve as means of increasing the genetic diversity of the offspring by multiple paternity.
To conclude, we can state that O. However, the latter reproduces obligately asexually, while the observed asexuality in O. We assume that at least some other cambarid crayfish may also be capable of switching to this reproductive mode. The capability of asexual reproduction may increase the chances of withstanding unfavourable conditions when sexual reproduction is not possible, or colonising new habitats from a small initial number of specimens.
While it remains unclear whether a single or several females of facultative parthenogenetic crayfish can establish a viable population without males, the reproductive plasticity of the spiny-cheek crayfish and possibly other cambarids apparently makes them less prone to various eradication techniques. For example, the sterile male release technique, recently suggested to be efficient for Procambarus clarkii  , may be ineffective for lower population densities if females switch to clonal reproduction instead of seeking mates, or after mating with a sterile mate.
Our findings confirm that cambarid crayfish, a serious threat to not only European freshwater ecosystems, are extremely well adapted to invasions. They were acclimated sexes separated to laboratory conditions for one month and placed in experimental tanks in September Ninety mature females and 45 mature males, randomly selected from these captured and acclimated animals, were used in the experiment.
All these specimens were in the sexually active form I in accordance with glair gland development in females, and the presence of form I copulatory stylets in males  ,  at the beginning of the experiment. The animals were divided into three experimental groups. Two groups consisted of thirty females and fifteen males that were allowed to move freely in their tanks.