Niche Shifts, Hybridization, Polyploidy and Geographic Parthenogenesis in Western North American Hawthorns (Crataegus subg. Sanguineae, Rosaceae)

We compare biogeographic and morphological parameters of two agamic complexes of western North American hawthorns so as to evaluate possible explanations of the differences in range between sexually reproducing taxa and their apomictic sister taxa. We have documented range, breeding system, morphology, leaf vascular architecture, and niche breadth in these hawthorns, for which phylogenetic relationships and ploidy levels are known. Species distribution data from herbarium specimens and online databases were analyzed in order to compare ranges and climate niches described by bioclimatic variables. Flow cytometry documented ploidy level and breeding system. Voucher specimens provided morphometric data that were analyzed using uni- and multivariate methods. Members of two black-fruited taxonomic sections of Crataegus subg. Sanguineae (sections Douglasianae, Salignae) have previously been identified as hybrids. They are presumptively self-fertile polyploids with pseudogamous gametophytic apomixis. Their morphologies, geographic ranges, and niche characteristics resemble those of their diploid, sexual parent or are intermediate between them and those of their other parent, one or both of two partially sympatric tetraploid apomicts in red-fruited C. subg. Americanae with much wider distributions. Comparing sections Douglasianae and Salignae suggests that geographic parthenogenesis (larger range sizes in apomicts, compared to sexually reproducing taxa) may have less to do with adaptation than it does with reproductive assurance in the pseudogamously apomictic and self-compatible hybrids. Greater climate niche breadth in allopolyploids compared to diploids similarly may be more due to parental traits than to effects of genome duplication per se.

Geographic parthenogenesis in the brown alga Scytosiphon lomentaria (Scytosiphonaceae): sexuals in warm waters and parthenogens in cold waters

Geographic parthenogenesis (GP), a phenomenon where parthenogens and their close sexual relatives inhabit distinct geographic areas, has been considered an interesting topic to understand the adaptation to marginal habitats and the role of hybridization in evolution. Reports of GP from land and freshwater are numerous, however, this occurrence has been rarely reported on from the sea. Brown algae are mostly marine and are thought to include numerous obligate parthenogens; still, little is known about the distribution, origin, and evolution of parthenogens in this group. Here we report a novel pattern of GP in the isogamous brown alga Scytosiphon lomentaria. Sex ratio investigation demonstrated that, in Japan, sexual populations grew in the coast along warm ocean currents, whereas female-dominant parthenogenetic populations grew mainly in the coast along a cold ocean current. In the two localities where sexual and parthenogenetic populations were parapatric, parthenogens grew in more wave-exposed areas than sexuals. Population genetic and phylogenetic analyses, including those based on genome-wide single nucleotide polymorphism data, suggested that: (1) parthenogens evolved at least twice in S. lomentaria, (2) parthenogens did not originate from inter-species hybridization, (3) new parthenogenetic lineages have arisen from hybridizations between parthenogens and sexuals, and (4) parthenogens have a wider distribution than sexuals. We also showed that the production of sex pheromones, which attract male gametes, has been independently suppressed/lost in two parthenogenetic lineages. This parallel suppression/loss of the sexual trait may represent the direct origin of parthenogens, or the regressive evolution of a useless trait under asexuality.

The Alternative Distribution of Related Earthworms Aporrectodea caliginosa and A. trapezoides (Oligochaeta, Lumbricidae) in Ukraine as a Case of Geographical Parthenogenesis

Geographical parthenogenesis describes phenomenon when parthenogenetic hybrid forms or species have larger distribution areas or higher abundance than their amphimictic parental species, especially in climatically unfavorable conditions. This phenomenon was studied in Ukraine for the pair species of earthworms Aporrectodea сaliginosa (Savigny, 1826) s. l. We found that the hermaphroditic amphimictic A. caliginosa clearly predominates in the northern and western regions, and the apomictic parthenogenetic A. trapezoides (Duges, 1828) in the southern and eastern regions with a continental arid climate. In the sample sets of A. сaliginosa–A. trapezoides group, usually one of the species sharply predominated, and the equality of their abundance was very rare. The reason for this fact is both the alternative geographical distribution and the ability of A. trapezoides to form populations in habitats unfavorable for A. caliginosa. In general, the situation in this group agrees with the classical model of geographic parthenogenesis and confirms the high adaptive potential of apomictic organisms. This fact once again raises the question of non-adaptive reasons for the exclusion of the apomictic reproduction in highly organized animals.

Parthenogenesis

The dominant mode of reproduction in eucaryotes is sexual. This has been described as a paradox given that sex is much more costly than reproducing asexually, such as by parthenogenesis. In the Crustacea, parthenogenesis is commonly found in the Ostracoda and Branchiopoda (Artemia and Cladocera), and studies of these species have made important contributions to understanding the ecological and evolutionary relationship between sexual and asexual reproduction. With respect to parthenogenesis, researchers have explored its taxonomic distribution and phylogeny, origin and mode, ecological genetics, and genomic signatures. Parthenogenetic Crustacea include both diploid and polyploid clones that have originated multiple times from related sexual species but appear to have a relatively limited evolutionary lifespan. Darwinulid ostracods may be one exception, with no known sexual forms and possibly an example of ancient asexuality, although this is controversial. Most parthenogenetic crustacean groups appear to have a wider geographic distribution than related sexual species and are often found in marginal habitats associated with higher latitudes and altitudes. Such patterns of geographic parthenogenesis have yet to be fully explained, but could possibly be due to colonization and adaptation advantages of asexuality; further studies are required to eliminate polyploidy alone as an explanation. There are many examples of parthenogenetic ostracods, cladocerans, and Artemia showing high levels of genetic diversity likely due to recent multiple origins from related sexual species. Phylogenetic analyses support this explanation and for Artemia and Daphnia, cases have been documented for rare functional males produced by parthenogenetic females that can mate with sexual females as a mechanism for generating new clonal lineages. The diversity of asexual species, combined with prior ecological and genetic information, suggests that crustaceans will continue as important models for understanding parthenogenesis, particularly with the application of new genomic tools.

Ecological success of sexual and asexual reproductive strategies invading an environmentally unstable habitat

Many aspects of sexual and asexual reproduction have been studied empirically and theoretically. The differences between sexual and asexual reproduction within a species often lead to a biased geographical distribution of individuals with different reproductive strategies. While sexuals are more abundant in the core habitat, asexuals are often found in marginal habitats along the edge of the species distribution. This pattern, called geographic parthenogenesis, has been observed in many species but the mechanisms reponsible for generating it are poorly known. We used a quantitative approach using a metapopulation model to explore the ecological processes that can lead to geographic parthenogenesis and the invasion of new habitats by different reproductive strategies. We analyzed the Allee effect on sexual populations and the population sensitivity to environmental stress during the invasion of a marginal, unstable habitat to demonstrate that a complex interaction between the Allee effect, sensitivity to environmental stress and the environmental conditions can determine the relative success of competing reproductive strategies during the initial invasion and longterm establishment in the marginal habitat. We discuss our results in the light of previous empirical and theoretical studies.Author SummaryIndividuals can reproduce with or without sex. Very often, closely related species are distributed in a such a way that the sexually reproducing species is most frequently found in the core habitat while the asexually reproducing species is found on the edge of the habitat range. This biased distribution of reproductive strategies across a habitat range is called geographic parthenogenesis and has been observed in several species. While many processes have been proposed to explain such a pattern, a quantitative approach of the ecological processes was absent. We investigated important differences between sexual and asexual reproduction and how these differences affect the success of sexuals and asexuals invading a marginal, unstable environment. We showed that the relative frequency of each reproductive strategy in the marginal habitat depends on how much sexuals rely on population density to reproduce and how much asexuals are affected by environmental stress relative to sexuals. Our study presents a quantitative ecological explanation for geographic parthenogenesis and provides the conditions under which different distribution patterns can emerge.

Asexual parasites and their extraordinary host ranges

In diverse parasite taxa, from scale insects to root-knot nematodes, asexual lineages have exceptionally large host ranges, larger than those of their sexual relatives. Phylogenetic comparative studies of parasite taxa indicate that increases in host range and geographic range increase the probability of establishment of asexual lineages. At first pass, this convergence of traits appears counter-intuitive: intimate, antagonistic association with an enormous range of host taxa correlates with asexual reproduction, which should limit genetic variation within populations. Why would narrow host ranges favor sexual parasites and large host ranges favor asexual parasites? To take on this problem I link theory on ecological specialization to the two predominant hypotheses for the evolution of sex. I argue that both hypotheses predict a positive association between host range and the probability of invasion of asexual parasites, mediated either by variation in population size or in the strength of antagonistic coevolution. I also review hypotheses on colonization and the evolution of niche breadth in asexual lineages. I emphasize parasite taxa, with their diversity of reproductive modes and ecological strategies, as valuable assets in the hunt for solutions to the classic problems of the evolution of sex and geographic parthenogenesis.

What does the geography of parthenogenesis teach us about sex?

Theory predicts that sexual reproduction is difficult to maintain if asexuality is an option, yet sex is very common. To understand why, it is important to pay attention to repeatably occurring conditions that favour transitions to, or persistence of, asexuality. Geographic parthenogenesis is a term that has been applied to describe a large variety of patterns where sexual and related asexual forms differ in their geographic distribution. Often asexuality is stated to occur in a habitat that is, in some sense, marginal, but the interpretation differs across studies: parthenogens might not only predominate near the margin of the sexuals' distribution, but might also extend far beyond the sexual range; they may be disproportionately found in newly colonizable areas (e.g. areas previously glaciated), or in habitats where abiotic selection pressures are relatively stronger than biotic ones (e.g. cold, dry). Here, we review the various patterns proposed in the literature, the hypotheses put forward to explain them, and the assumptions they rely on. Surprisingly, few mathematical models consider geographic parthenogenesis as their focal question, but all models for the evolution of sex could be evaluated in this framework if the (often ecological) causal factors vary predictably with geography. We also recommend broadening the taxa studied beyond the traditional favourites. This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.