Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing.
Here, we present the results of a new comparative study based exclusively on the ancient asexual clades. association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades.
Using the conservative definition of ancient asexuals i. The difference between the environmental type associated with the sexual and asexual species was then compared in an exact binomial test.
The results showed that the majority of ancient asexual clades tend to be associated with biotically, abiotically, or both biotically and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos, and soil.
The consequences of these findings for the ecological theories of sexual reproduction are discussed. Sexual reproduction sensu amphimixis, the alternation of meiosis and syngamy is one
Asexual definition biologia general the most enigmatic phenomena in evolutionary biology see, e. None of these Asexual definition biologia general apply to all sexual species because of the highly variable nature of their reproduction.
Many main concepts and their countless variants were proposed to explain the paradox of sexual reproduction reviewed, e. Ecological theories of sexual reproduction, on the other hand, stress the assumption that sex provides some ecological advantage to sexual species. Sex is obviously not universally advantageous. The difference lies mainly in their target of interest. The speed, not the depth, of adaptation is more important in these environments Maynard Smith, A classification of ecological theories of the maintenance of sexual reproduction presented in this paper.
Given the extraordinary plethora of proposed concepts, this summary cannot be exhaustive nor complete. Only the major concepts as they were originally proposed are included. Main characteristics of biotically and abiotically heterogeneous environments in the optics of ecological theories of sexual reproduction and examples of habitats that are characteristic by strong biotic and abiotic heterogeneity.
Another group of ecological theories of sexual reproduction comprises, for example, the lottery and Sisyphean genotypes hypothesis Williams,elbow room hypothesis Maynard Smith,tangled bank hypothesis Bell,hypothesis of fluctuating selection Smith,and hypothesis of reduced response to fluctuating selection Roughgarden, Under these circumstances, the asexual species might have an advantage because, for example, they do not suffer from segregation and recombination loads Crow, However, the spatial and temporal heterogeneity of an environment is expected to usually ensure the advantage of sexual species.
The "Asexual definition biologia general" of the environment, both biotic and abiotic, can be comprehended as the sum of heterogeneity in space in the sense of variability, e. In principle, the most important factor is always whether the environment inhabited by the offspring differs in its character i. According to the major source of the environmental heterogeneity, it is therefore essentially possible to differentiate between these two groups of ecological theories of sexual reproduction.
However, the predictions of different theories are not absolutely disparate—one could easily devise examples of environments suitable for asexual species according to both groups of theories, Asexual definition biologia general example, stable extreme environments.
Ecological theories of sexual reproduction and their predictions regarding environmental heterogeneity. Diagram illustrating predictions of ecological theories of sexual reproduction regarding environmental heterogeneity. This is in stark contrast with several concepts that consider both kinds of environmental heterogeneity important for promoting sexual reproduction green.
Color saturation indicates hypothetical advantage of sexual organisms over asexuals in given conditions according to each group of theories. Such alleles as well as alleles that are pleiotropically or epistatically interconnected with them are not easily fixated or eliminated. Therefore, it is possible that sexual species, in contrast to asexual ones, are usually not able to fully adapt to transient environmental changes; they mostly retain some genetic polymorphism that helps them escape extinction when the conditions quickly return to normal.
It was suggested by Williams pp. Given the similarities between the effect Asexual definition biologia general temporal and spatial heterogeneity mentioned above, this notion can be readily extended to encompass both temporal and spatial heterogeneity.
Similar remarks were made, for example, by Williamsp. Most of the organisms that live on Earth, Archaea and Bacteria, are primarily asexual. The primary asexuality is a plesiomorphic trait and therefore does not need any special explanation. It therefore possible to compare the environmental biotic heterogeneity and abiotic heterogeneity of such secondary asexual clades with that of their sexual relatives to test particular ecological hypotheses of sexual reproduction.
Most studies aimed at testing and discriminating between individual ecological theories of sexual reproduction on the basis of their predictions about the environmental correlates of sexual and asexual lineages showed largely inconclusive results.
Often their aim was to test particular theoretical concepts: The most extensive comparison not focused on testing one particular theoretical concept was performed by Bell on multicellular animals Metazoa. It mostly supported the tangled bank hypothesis. Experiments aimed at discriminating the selective pressures of biotically see, e.
However, particular mechanisms that favor higher levels of sex are hard to determine in these cases that are, moreover, often based on facultatively sexual organisms. The main problem of the comparative studies mentioned above may be the inclusion of both old and young asexual taxa. In the first part of the study, we compiled data on the environmental heterogeneity of AAs and their sexual controls. In the second, analytical, part of the study, we used the data to test whether AAs more often inhabit 1 generally less heterogeneous environments, 2 less biotically heterogeneous environments, or 3 less abiotically heterogeneous environments.
To this end, we used paired exact tests to compare the ecological demands of sexual species and AA species within unrelated clades of eukaryotic organisms. In the third, exploratory, part of the study, we "Asexual definition biologia general" for particular environmental properties and organismal adaptations that are common among the AA members of the pairs. This is the main reason that our study is based exclusively on AAs as they already proven to be evolutionarily viable in the long term.
However, it is worth mentioning that the focus on AAs puts forward another serious difficulty: These clades were separated from their sister sexual lineages a long time ago at least 1 million years ago, see Materials and Methodsand both sexual and asexual lineages thus underwent considerable time periods of independent evolution. Therefore, both lineages independently acquired numerous adaptations that distinguished them but need not be related to the mode of their reproduction.
Some researchers consider a lineage to be AA if it reproduces obligately asexually for at least 50, generations or 0. It is not the aim of this study to argue for the substantial difference of AAs from other asexuals or against it. We focus only on groups that were proven to survive exclusively in an asexual state for a considerable amount of time.
Thus, regardless of the discussion on the fundamental distinction of young and old asexual taxa, in the current study we defined AAs conservatively as those secondary asexual eukaryotic lineages that reproduce obligately asexually with a great deal of certainty for at least one million years see Table S1 for details. The evidence for confirmation or rejection of putative AAs included organismal, life history, palaeontological, biogeographical, molecular, individual genetic, and population genetic data and also other indices of ancient asexuality proposed in the AA literature listed above.
The list of supported and contested AA candidates, as well as reasons for our decision, is summarized in Table S1. In the next step, we identified ecologically comparable sexual sister lineages for the eight AA groups using literary sources. In those individual cases in which the phylogenetic relations between the sexual and asexual lineages were not entirely clear, we used the closest possible comparable clades see Table S2 for details.
The remaining AA groups were polyphyletic, that Asexual definition biologia general, they included several related monophyletic asexual sublineages with interstitial sexual lineages. We treated each of these groups as single unit in the analysis. In these cases, we compared every individual AA lineage with its sexual control in the monophyletic subtaxa of the polyphyletic AA group and based our conclusions on the prevailing trend i.
With the exception of Timemathe internal phylogenetic relationships of the studied polyphyletic AA groups were more or less unclear.
Where possible, we proceeded using the most probable relationships Bdelloidea, Darwinulidae, Oribatidae, Nematalycidae and Proteonematalycidae, Grandjeanicidae, and Oehserchestidae, see Table S2. Comparison of the biotic "Asexual definition biologia general" abiotic heterogeneity of an environment inhabited by the studied ancient asexuals and their sexual controls. Asexual definition biologia general
Detailed evaluation of the habitat heterogeneity is given in each pair to support our decision of which member of the pair inhabits a biotically or abiotically more Asexual definition biologia general environment.
Biotic and abiotic environmental heterogeneity clearly have a nontrivial relationship to each other see Discussionbut it is essentially possible to distinguish them.
It is also worth mentioning that an environmental heterogeneity, both biotic and abiotic, is an emergent property stemming from different factors and different adaptations in various AAs. An environmental heterogeneity of microscopic and macroscopic organisms, or more generally organisms living on Asexual definition biologia general spatiotemporal scales, eventually organisms with completely different ecological strategies terrestrial, benthic, planktonic, parasitic etc. However, individual AAs and their ecologically comparable sexual controls can be compared on the basis of particular factors that indicate a higher or a lower biotic or abiotic environmental heterogeneity of their particular environment.
Resulting binary data were possible to analyze statistically. Summary of factors that were evaluated Asexual definition biologia general determine a higher or a lower environmental heterogeneity of AAs in comparison with their sexual controls. See Supporting information Materials and Methods for commentary and detailed description on how we determined biotic and abiotic environmental heterogeneity. Collected data were analyzed using the R v. We used an exact test suggested by R.
Using this technique, we tested three hypotheses: In case, the heterogeneity of habitats of AAs and their sexual controls differ, then asexual members of the pairs inhabit predominantly 1 biotically or abiotically, 2 biotically, and 3 abiotically more homogeneous environments.
Only in two AA groups LasaeaTimemawe were unable to identify any consistent differences in the heterogeneity of the environments inhabited by their sexual and asexual lineages. The most probable explanation of the absence of such a difference is a lack of empirical data. As the tested hypothesis makes predictions only about those "Asexual definition biologia general" of species that differ in the heterogeneity of their habitats and the binomial test analyses only binary variables, i.
The same applies for the abiotic heterogeneity of environment of Darwinulidae. The ecology, relevant adaptations, and environmental correlates of all eight pairs of AAs and their sexual controls were thoroughly examined in the exploratory part of the study, see Discussion.
We conclude that eight of the putative AA groups do fulfill our strict criteria of ancient asexuality: Their sister or closely related ecologically comparable sexual groups were identified consequently with the help of relevant literature; see Table S2. All these results are statistically significant. In the exploratory part of the study, we searched for the traits that could be typical for ancient asexual organisms.
The most notable are durable resting stages, life in benthos and soil, and life in the absence of intense biotic interactions. The distribution of specific environmental properties and organismal adaptations associated with studied AA taxa.
Significance of these findings is discussed below. In contrast with other comparative studies in the field, the presented one is based exclusively on the AA taxa.