Evolution in the slow lane: molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda)

Parthenogenetic lineages within non-marine ostracods can occur either in mixed (with sexual and asexual females) or exclusively asexual taxa. The former mode of reproduction is associated with a high intraspecific diversity at all levels (genetic, morphological, ecological) and, at least in the Cypridoidea, with geographical parthenogenesis. Obligate asexuality is restricted to the Darwinuloidea, the strongest candidate for an ancient asexual animal group after the bdelloid rotifers, and is characterized by low diversity. We have compared rates of molecular evolution for the nuclear ITS1 region and the mitochondrial COI gene amongst the three major lineages of non-marine ostracods with sexual, mixed and asexual reproduction. Absolute rates of molecular evolution are low for both regions in the darwinulids. The slow-down of evolution in ITS1 that has been observed for Darwinula stevensoni (Brady & Robertson) apparently does not occur in other darwinulid species. ITS1 evolves more slowly than COI within non-marine ostracod families, including the darwinulids, but not between superfamilies. The ancient asexuals might have a higher relative substitution rate in ITS1, as would be expected from hypotheses that predict the accumulation of mutations in asexuals. However, the speed-up of ITS could also be ancient, for example through the stochastic loss of most lineages within the superfamily after the Permian–Triassic mass extinction. In this case, the difference in rate would have occurred independently from any effects of asexual reproduction.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 93–100.     

Transposable elements in clonal lineages: lethal hangover from sex

Long-term coevolution of transposable elements (TEs) in sexual hosts leads to evolution of extremely active and dangerous mutagens kept in tenuous check by host-derived mechanisms and via natural selection against TE-rich genomes. To the extent that sexual reproduction and recombination are important in maintaining a stable TE copy number and a tolerable mutation load, the switch to clonality from sexual reproduction can be extremely damaging and, generally, should lead to clonal lineage extinction. Surprisingly however, the loss of powerful selective mechanisms constraining TEs can be beneficial in the short-term by immediately eliminating selective load and possibly promoting the early success of clonal lineages. The clonal lineages that do survive in the long-term must find a way to eliminate or domesticate TEs. Indeed bdelloid rotifers, which are ancient asexuals, do appear to have lost most of the otherwise wide-spread TEs and might have domesticated others. The path to this TE-free haven is anything but clear at the moment. We have considered a novel scenario of instantaneous inactivation of TEs by starting off with a genome carrying repressive host alleles for all TEs in the genome. We show that such a scenario appears plausible and provide some limited empirical evidence in its support.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 33–41.     

Ancient asexual scandals

Asexual organisms that are descended from ancient asexual lineages defy current thinking on the evolution of sexual reproduction; theoreticians have been anxious to explain away their existence. However, a number of groups of organisms, from ferns to rotifers, have been suggested to be anciently asexual, and favourable evidence is being accumulated. Furthermore, new techniques for assessing claims of ancient asexuality have been proposed. Although ancient asexuals challenge current theories of sex, understanding how they manage to persist will help to explain why most organisms are sexual.     

Distribution, phenology and demography of sympatric sexual and asexual dandelions (Taraxacum officinale s.l.): geographic parthenogenesis on a small scale

In many plant and animal species, sexual and asexual forms have different geographical distributions ('geographic parthenogenesis'). The common dandelion Taraxacum officinale s.l. provides a particularly clear example of differing distributions: diploid sexuals are restricted to southern and central Europe, while triploid asexuals occur across Europe. To get a better understanding of the factors underlying this pattern, we studied the distribution and demography of sexuals and asexuals in a mixed population that was located at the northern distribution limit of the sexuals. In this population three adjacent, contrasting microhabitats were found: a foreland and south and north slopes of a river dike. Comparative analyses of the distribution, phenology and demography indicated that sexuals had a stronger preference for the south slope than did asexuals. We therefore propose that the large-scale geographic parthenogenesis in T. officinale is shaped by an environmental gradient which acts upon the sexuals.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 205–218.     

Direct and indirect selection in moth pheromone evolution: population genetical simulations of asymmetric sexual interactions

Female moths generally use pheromones to attract males. Normally, all females in a population produce a specific chemical blend with only a limited variance, and the local males are highly attracted to this blend. To better understand the direct and indirect selective forces acting on this communication system, where, unusually, it is the reproductively limited sex that signals for matings, a population genetical model has been constructed and numerically analysed. Basic to the model is the assumption that the pheromone attraction system functions asymmetrically, leading to strong sexual selection between males but no direct sexual selection between females. Evolutionary simulations using the model show that sexual selection in males causes an indirect stabilizing selection on the pheromone blends produced by females. Thus, a more narrow range of pheromone variation is selected for, even in the absence of female sexual selection. The strength of the selection is analysed, and it is suggested that this indirect stabilizing selection becomes particularly important in situations where geographically adjacent populations have evolved different pheromone blends.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 117–123.     

Plant clonality, mutation, diplontic selection and mutational meltdown

Apomixis is a very common characteristic in vascular plants. It occurs in two general forms: either subversion of the sexual system (agamospermous seeds or apogamous sporophytes in non-seed plants) or vegetative reproduction. In this communication, only the mutational consequences of vegetative reproduction are considered. Vegetative reproduction involves the replication of apical meristems, especially shoot apical meristems. Three general types of shoot apical meristems occur in the vascular plants: single tetrahedral apical initial, unstratified with impermanent initials and stratified with impermanent initials. Each meristem type has different consequences with regard to mutation, diplontic selection and the possibility of mutational meltdown.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 61–67.     

Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality

Neutral models characterize evolutionary or ecological patterns expected in the absence of specific causal processes, such as natural selection or ecological interactions. In this study, we describe and evaluate three neutral models that can, in principle, help to explain the apparent 'twigginess' of asexual lineages on phylogenetic trees without involving the negative consequences predicted for the absence of recombination and genetic exchange between individuals. Previously, such phylogenetic twiggyness of asexual lineages has been uncritically interpreted as evidence that asexuality is associated with elevated extinction rates and thus represents an evolutionary dead end. Our first model uses simple phylogenetic simulations to illustrate that, with sexual reproduction as the ancestral state, low transition rates to stable asexuality, or low rates of ascertained 'speciation' in asexuals, can generate twiggy distributions of asexuality, in the absence of high extinction rates for asexual lineages. The second model, developed by Janko et   al . (2008 ), shows that a dynamic equilibrium between origins and neutral losses of asexuals can, under some conditions, generate a relatively low mean age of asexual lineages. The third model posits that the risk of extinction for asexual lineages may be higher than that of sexuals simply because asexuals inhabit higher latitudes or altitudes, and not due to effects of their reproductive systems. Such neutral models are useful in that they allow quantitative evaluation of whether empirical data, such as phylogenetic and phylogeographic patterns of sex and asexuality, indeed support the idea that asexually reproducing lineages persist over shorter evolutionary periods than sexual lineages, due to such processes as mutation accumulation, slower rates of adaptive evolution, or relatively lower levels of genetic variability.     

Polyploidy and the sexual system: what can we learn from Mercurialis annua?

The evolutionary success of polyploidy most directly requires the ability of polyploid individuals to reproduce and transmit their genes to subsequent generations. As a result, the sexual system (i.e. the mating system and the sex allocation of a species) will necessarily play a key role in determining the fate of a new polyploid lineage. The effects of the sexual system on the evolution of polyploidy are complex and interactive. They include both aspects of the genetic system, the genetic load maintained in a population and the ecological context in which selection takes place. Here, we explore these complexities and review the empirical evidence for several potentially important genetic and ecological interactions between ploidy and the sexual system in plants. We place particular emphasis on work in our laboratory on the European annual plant Mercurialis annua , which offers promising scope for detailed investigations on this topic. M. annua forms a polyploid complex that varies in its sexual system from dioecy (separate sexes) through androdioecy (males and hermaphrodites) to functional hermaphroditism.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 547–560.     

Sexual size dimorphism and sex ratios in dragonflies (Odonata)

Sexual size dimorphism and biased sex ratios are common in animals. Rensch's rule states that sexual size dimorphism (SSD) would increase with body size in taxa where males are larger than females and decrease with body size in taxa where females are larger. We tested this trend in dragonflies (Odonata) by analysing body size of 21 species and found support for Rensch's rule. The increase in SSD with increasing size among species can be explained by sexual selection favouring large males. We also estimated the slope of the relationship between sex ratio and size ratio in populations of the 21 species. A negative slope would suggest that the larger sex suffers from high mortality in the larval stage, consistent with riskier foraging. The slope of this relationship was negative, but after correcting for phylogentic non-independence with independent contrasts the relationship was no longer statistically significant, perhaps because of phylogenic inertia or low sample size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 507–513.     

Covariation between predation risk, body size and fin elaboration in the green swordtail, Xiphophorus helleri

Natural and sexual selection can have either opposing or synergistic effects on the evolution of traits. In the green swordtail Xiphophorus helleri , sexual selection arising from female choice is known to favour larger males and males with longer swords. We examined variation in male and female size and fin morphology among 15 populations that varied in their predation environments. Males and females from populations in which piscivorous fishes were present had longer and deeper bodies than did males and females from populations in which piscivorous fishes were absent. Controlling for a positive effect of body size on sword length, males from populations in which piscivores were present had relatively shorter swords than did males from populations in which piscivores were absent. The associations between morphology and predation environment may be due to direct effects of predation, indirect effects of predation, other sources of selection that covary with predator presence, or other environmental effects on trait expression. These results suggest that while sexual selection favours longer swords, natural selection may have an opposing effect on sword length in populations with predators. Natural selection on body size, however, may act synergistically with sexual selection in populations with predators; both may favour the evolution of larger body size. The body size results for X. helleri contrast with related taxa that have become model systems for the study of life history evolution.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 87–100.     

Limits to sexual size dimorphism in red‐winged blackbirds: the cost of getting big?

A fundamental assumption of sexual selection theory is that the reproductive advantage of large size is balanced by a survival disadvantage. Previous studies of the sexually size-dimorphic red-winged blackbird ( Agelaius phoeniceus ) have indicated that the largest adult males have a survival advantage, suggesting that the limit to male size may be the cost of getting big rather than the cost of being big. If the cost of getting big limits male size, then starvation rates for male nestlings should exceed those of female nestlings. In addition, given high heritability of body size, larger parents should lose more nestlings, particularly males, to starvation. We tested these predictions for red-winged blackbirds using data on the sex of 1356 fledglings from 465 nests collected over 10 years. We found no disadvantage for male nestlings relative to females – 49% of fledglings were male and previous research had shown that 48% of hatchlings are male. We also found no disadvantage for male nestlings that would become large adults (i.e. those with larger parents) – partial brood loss and fledging sex ratios did not vary with mid-parent size. Given no apparent disadvantage to large size for males either as adults or as nestlings, this leaves only the period between fledging and adulthood during which natural selection might limit sexual size dimorphism, although other mechanisms might explain the failure to find a limit to male size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 353–361.     

Quantification of sexual dimorphism in Asellus aquaticus (Crustacea: Isopoda) using outline approaches

A marked sexual dimorphism is often observed in arthropods species in which males perform precopulatory mate guarding. It is generally thought to reflect the influence of sexual selection. Until now, sexual dimorphisms associated with mate guarding have mainly been qualitatively described. However, assessing the effects of sexual selection on sexual dimorphims requires a preliminary quantitative assessment of differences in morphology between sexes. Using Fourier analyses, we tested if morphological dimorphisms could be quantitatively assessed in the isopod Asellus aquaticus . In addition, we checked whether sexual dimorphism in shape was exclusively related to mate guarding through considering characters that are not, a priori , implicated in mating behaviour. To assess the potential role of sexual selection in shaping morphology, we then examined how dimorphic characters could influence males' pairing success. Three characters (pleotelson, paraeopods 4 and 5) differed significantly in shape between males and females. In addition, two characters (pleotelson and paraeopods 4) differed in shape between guarding males and non-guarding males, with the latter being closer in shape to females. This suggests that sexual selection may be partly responsible for the observed morphological divergence between sexes in A. aquaticus .  © 2002 The Linnean Society of London, Biological Society of the Linnean Society , 2002, 77 , 523–533.     

The evolution of male genitalia: functional integration of genital sclerites in the dung beetle Onthophagus taurus

It is now widely recognized that sexual selection has been important in the rapid and divergent evolution of male genital morphology. However, distinguishing among putative mechanisms of sexual selection acting on male genital morphology represents a considerable challenge. Although there is growing evidence that variation in the size and/or shape of male genital structures can determine a male's success in gaining fertilizations, our knowledge of the functional morphology of male genitalia remains limited. Here we examine the functional morphology of genital sclerites that are known to influence paternity in the dung beetle Onthophagus taurus . We show that three of the sclerites form a functionally integrated unit that generates the tubular-shaped spermatophore and delivers its opening to the female's spermathecal duct. A fourth sclerite acts as a holdfast device during copulation. Our observations shed light on the mechanism by which these sclerites influence a male's paternity, and their patterns of phenotypic and genetic (co)variation.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 257–266.     

The fitness advantage of a high-performance weapon

Weapons used in combat between males are usually attributed to sexual selection, which operates via a fitness advantage for males with weapons of better 'quality'. Because the performance capacity of morphological traits is typically considered the direct target of selection, Darwin's intrasexual selection hypothesis can be modified to predict that variation in reproductive success should be explained by variation in performance traits relevant to combat. Despite such a straightforward prediction, tests of this hypothesis are conspicuously lacking. We show that territorial male collared lizards with greater bite-force capacity sire more offspring than weaker biting rivals but exhibit no survival advantage. We did not detect stabilizing or disruptive selection on bite-force capacity. Taken together, these results support the hypothesis that superior weapon performance provides a fitness advantage through increased success in male contests. Sexual selection on weapon performance therefore appears to be a force driving the evolution and maintenance of sexual dimorphism in head shape.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 840–845.     

High levels of genetic diversity in populations of Iris aphylla L. (Iridaceae), an endangered species in Poland

We used RAPDs (Random Amplified Polymorphic DNAs) to investigate genetic diversity and its partition within and between three populations of Iris aphylla in Poland. Analysis of Molecular Variance (AMOVA) of 84 distinct RAPD multiband genotypes revealed higher variation within populations (77.2%) than genetic differentiation between them (22.8%, P  < 0.002). Values of genetic diversity indices ( H ) were similar in all three sites (0.21–0.24). The differentiation of the populations corresponded to low average gene flow ( Nm  = 0.81). Our results indicated that genetic diversity was independent of population size. We concluded that although sexual reproduction and gene flow between populations of I. aphylla were very limited, they preserved high levels of genetic diversity. Relatively large number of seeds, which migrated in the past to populations, as well as patterns of reproduction and life history of I. aphylla may explain this situation.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 142 , 65–72.     

Molecular evidence for ancient asexuality in timema stick insects

Asexuality is rare in animals in spite of its apparent advantage relative to sexual reproduction, indicating that it must be associated with profound costs [1-9]. One expectation is that reproductive advantages gained by new asexual lineages will be quickly eroded over time [3, 5-7]. Ancient asexual taxa that have evolved and adapted without sex would be "scandalous" exceptions to this rule, but it is often difficult to exclude the possibility that putative asexuals deploy some form of "cryptic" sex, or have abandoned sex more recently than estimated from divergence times to sexual relatives [10]. Here we provide evidence, from high intraspecific divergence of mitochondrial sequence and nuclear allele divergence patterns, that several independently derived Timema stick-insect lineages have persisted without recombination for more than a million generations. Nuclear alleles in the asexual lineages displayed significantly higher intraindividual divergences than in related sexual species. In addition, within two asexuals, nuclear allele phylogenies suggested the presence of two clades, with sequences from the same individual appearing in both clades. These data strongly support ancient asexuality in Timema and validate the genus as an exceptional opportunity to attack the question of how asexual reproduction can be maintained over long periods of evolutionary time.     

Rapid divergence of social signal coloration across the White Sands ecotone for three lizard species under strong natural selection

Animal social signals are important for population recognition, communication, and mate choice. Although natural selection often favours cryptic coloration, sexual selection can underlie patterns of coloration that function in inter- or intrasexual communication. We compared social signal coloration of three lizard species across a substrate colour ecotone in New Mexico. These species exhibit cryptic blanched dorsal coloration on the gypsum dunes of White Sands and dark coloration on the surrounding desert soils. We detected corresponding population divergence in colour used for intra- ( Aspidoscelis inornata , Sceloporus undulatus ) or inter- ( Holbrookia maculata ) sexual signalling. Although the magnitude and direction of change in coloration varied among taxa, differences in hue and chroma accounted for more variation in social coloration than for dorsal coloration. The relative conspicuousness of social signals also varied across the ecotone. We discuss the possibilities that divergent signalling colours in this system are the result of: (1) stochastic processes, (2) direct selection, and/or (3) a correlated response to natural selection on dorsal coloration.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 243–255.     

Recent and ancient asexuality in Timema walkingsticks

Determining the evolutionary age of asexual lineages should help in inferring the temporal scale under which asexuality and sex evolve and assessing selective factors involved in the evolution of asexuality. We used 416 bp of the mitochondrial COI gene to infer phylogenetic relationships of virtually all known Timema walkingstick species, including extensive intraspecific sampling for all five of the asexuals and their close sexual relatives. The asexuals T. douglasi and T. shepardii were very closely related to each other and evolutionarily young (less than 0.5 million years old). For the asexuals T. monikensis and T. tahoe, evidence for antiquity was weak since only one population of each was sampled, intraspecific divergences were low, and genetic distances to related sexuals were high: maximum-likelihood molecular-clock age estimates ranged from 0.26 to 2.39 million years in T. monikensis and from 0.29-1.06 million years in T. tahoe. By contrast, T. genevieve was inferred to be an ancient asexual, with an age of 0.81 to 1.42 million years. The main correlate of the age of asexual lineages was their geographic position, with younger asexuals being found further north.     

Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals

In theory, parthenogenetic lineages have low evolutionary potential because they inexorably accumulate deleterious mutations and do not generate much genotypic diversity. As a result, most parthenogenetic taxa occupy the terminal nodes of phylogenetic trees. The rate and mode of development of parthenogenesis are important factors to consider when assessing its costs and benefits since they determine both the level of genetic diversity and the ecological adaptability of the resulting lineages. The origin of parthenogenesis is polyphyletic in many taxa, suggesting that genetic systems maintaining sexuality are often labile. In addition, the loss of sex may be achieved in several ways, leading to parthenogenetic lineages with distinct genetic profiles. This could then influence not only the fate of such lineages in the long term, but also the outcome of competition with their sexual counterparts in the short term. In this paper, we review the possible evolutionary routes to parthenogenesis based on a survey of the phylogenetic relationships between sexual and parthenogenetic lineages in a broad range of animals. We also examine the different mechanisms by which parthenogenetic lineages could arise, and discuss the influence of these mechanisms on both the genetic properties and the ecological life styles of the resulting lineages.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 151–163.