[show abstract][hide abstract] ABSTRACT: Copulation can involve the wounding of the mating partner by specialised devices. This type of mating, which we term traumatic mating, has been regarded as exceptional. Its prevalence, however, has not been compared across taxa, nor have its functions and putative evolutionary pathways. A categorisation has been lacking to date. We here show that traumatic mating is a widespread and diverse phenomenon that likely evolved via several pathways. Its putative functions include: (i) anchorage during mating; (ii) stimulation of short-term female reproductive investment; (iii) male paternity advantages; and (iv) enhanced fertilisation efficiency in transitions to internal fertilisation. Both natural and sexual selection have likely contributed to the parallel evolution of traumatic intromittent organs in phylogenetically distant taxa. These organs are sometimes remarkably similar in shape and often, but not always, inject sperm. The target sites of trauma infliction and the nature of secretions delivered alongside sperm are thus far poorly studied, but data on both are needed to elucidate the function of traumatic mating. The few existing studies that explicitly quantify fitness impacts of traumatic mating indicate that this strategy may often be costly to the party being wounded. However, a comprehensive approach to assess overall investments and returns for both sexes is a major target for future work. Finally, for the first time, we corroborate quantitatively the hypothesis that traumatic mating evolved relatively more often among hermaphroditic than among gonochoric taxa.
[show abstract][hide abstract] ABSTRACT: The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite-mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male-mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.
[show abstract][hide abstract] ABSTRACT: 1.Sexual populations are expected to perform better in fluctuating environments than asexuals because recombination provides the potential to adapt to changing environments due to increased genetic variation. Nevertheless, some asexual species show comparably high levels of genotypic diversity. Such diversity might be achieved through gene flow between coexisting sexual and asexual populations or through sexual events within asexual populations. 2.Evidence for occasional sex in the flatworm Schmidtea polychroa was previously found at one specific site that is inhabited by parthenogenetic forms. There, varying rates of sex between subpopulations, reaching up to 12%, were observed. Past recurrent sexual processes left a significant genetic signature in the population genetic structure of this population. In the present study, we examined the population genetic structure of six independent metapopulations (lakes) of the freshwater planarian flatworm S. polychroa, to confirm the presence of occasional sex and that its population genetic consequences can be generalised. 3.Using microsatellites, we found varying rates of occasional sex among subpopulations. Metapopulations showed medium to high levels of genotypic diversity that correlated with the rate of sex. 4. We conclude that occasional sex has considerable consequences for population genetic structure of parthenogenetic species and promotes diversity that might allow response to the particular type of selection that is usually predicted to favour sexual reproduction. This reproductive strategy provides genetic characteristics required for selection to act on, and might, therefore, explain the success of this parthenogenetic species.
[show abstract][hide abstract] ABSTRACT: Contrary to many separate sex systems, the evolutionary ecology of polyandry in simultaneous hermaphrodites, and in particular
in those with internal fertilization, has received little attention. Recent studies on the promiscuous gastropod Chelidonura sandrana showed that offspring size, an important determinant of offspring performance in many marine invertebrates, varies with the
number of different mating partners. However, the source of this differential allocation by mothers remained unclear. Using
a quantitative genetic model, we here tested for parental effects on offspring size and the importance of ‘good gene’ effects
on early life history traits. Our analysis revealed no significant sire but strong dam effects for all investigated traits.
Moreover, embryo viability tended to increase with egg capsule volume, thus linking offspring size with offspring performance.
Our findings suggest that in C. sandrana (1) differential allocation is a maternal effect in response to the number of different partners, and that (2) additive genetic
variance is of negligible importance in early life history traits.
[show abstract][hide abstract] ABSTRACT: Intraspecific variation in mating behavior is widespread among simultaneous hermaphrodites but its underlying sources remain
largely unexplored. In the sea slug Chelidonura sandrana, most matings are reciprocal. However, despite non-conditional sperm exchange and potential polygamy-mediated benefits, 30%
of matings end after unilateral insemination. To resolve this apparent inconsistency, we here investigated the effect of body
size on the frequency of reciprocal matings by testing the following two hypotheses. First, sex-allocation theory predicts
that the likelihood of reciprocity depends on the size difference between mating partners. Second, if both sex functions temporally
differ in reaching maturity, reciprocal matings should be more frequent with increasing absolute body size of the smaller
partner. The likelihood of reciprocity increased with body size of the smaller partner. Moreover, smaller individuals acted
more often as males among unilateral matings. These findings suggest that the ability to donate sperm develops prior to female
functionality in C. sandrana.
Behavioral Ecology and Sociobiology 04/2012; 63(6):953-958. · 2.75 Impact Factor
[show abstract][hide abstract] ABSTRACT: Most heat shock proteins help to cope with stress in organisms ranging from bacteria to vertebrates. Many stress types acting
on the intensity of intracellular protein can induce expression of heat shock proteins. Here, we studied changes in expression
level of heat shock protein 70 (Hsp70), one of the best investigated stress proteins, in response to five potential stress
factors in the planarian flatworm Schmidtea polychroa: (1) homogenized planarian tissue, which releases an alarm substance that signals predation injury, (2) physical damage by
puncturing, (3) a simulation of ecological competition by adding a mixture of naturally co-occurring species: one Dendrocoelum and two Polycelis flatworms, one Asellus water louse and one leech, and (4) magnesium chloride, which inhibits regeneration ability. We found that alarm substance
(1), physical harm (2), and magnesium chloride (4) led to increased expression of Hsp70, while interspecific competition (3)
did not result in elevated Hsp70 expression. There was no difference between the experimental negative control and two temporal
controls immediately after collection and just before the experiment. Results show that Schmidtea polychroa is not sensitive to sampling and lab maintenance. However, planarian homogenate, magnesium chloride and physical harm all
caused Hsp70-inducing stress. We conclude that Hsp70 quantification is appropriate to study the current stress level in planaria
in response to specific conditions.
[show abstract][hide abstract] ABSTRACT: Offspring size can have pervasive effects throughout the life history stages of many marine invertebrates. Although maternal
offspring investment is largely determined by the environmental conditions experienced by the mother, egg size might additionally
vary in response to the number and quality of previous mating partners. Positive effects of mating multiply with several different
males (polyandry) have been confirmed for a variety of species, whereas such investigations are lacking for marine invertebrates.
Here we differentiated between the effects of ejaculate amount (repeatedly mated) and ejaculate diversity (polyandry) on maternal
offspring investment in the simultaneously hermaphroditic sea slug Chelidonura sandrana. We found that focal “females” mated with four different “males” produced significantly larger egg capsules and larger veligers,
while focal “females” mated four times with the same “male” suffered from reduced mid-term fecundity. We found no effect of
veliger size on veliger survival. Our results show that female mating patterns are an important addition to understanding
the variation in offspring size in internally fertilizing marine invertebrates.
[show abstract][hide abstract] ABSTRACT: Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.
Behavioral Ecology and Sociobiology 04/2012; 60(3):359-367. · 2.75 Impact Factor
[show abstract][hide abstract] ABSTRACT: Sexual conflict between mating partners can give rise to strategies that are advantageous for one sex but harmful to the opposite sex. Usually, sperm donors develop (offensive) traits to enhance their chances in sperm competition, while sperm recipients evolve (defensive) traits that allow them to stay in control of who fathers their offspring. Here, we demonstrate that these processes are also at work in simultaneous hermaphrodites. The hermaphroditic earthworm Lumbricus terrestris uses 40 to 44 copulatory setae to pierce into its partner's skin, causing damage and injecting a substance from its setal glands. Experimental injection of the gland substance indicates that a refractory period may be induced. More importantly, removal of the copulatory setae shows that they influence the partner's sperm uptake. When the setae are present, more sperm are taken up and sperm are distributed more equally over the four spermathecae. We interpret this as a strategy that stacks the odds for the donor's sperm in fertilizing cocoons.
Behavioral Ecology and Sociobiology 04/2012; 59(2):243-249. · 2.75 Impact Factor
[show abstract][hide abstract] ABSTRACT: Body coloration plays a major role in fish ecology and is predominantly generated using two principles: a) absorbance combined with reflection of the incoming light in pigment colors and b) scatter, refraction, diffraction and interference in structural colors. Poikilotherms, and especially fishes possess several cell types, so-called chromatophores, which employ either of these principles. Together, they generate the dynamic, multi-color patterns used in communication and camouflage. Several chromatophore types possess motile organelles, which enable rapid changes in coloration. Recently, we described red fluorescence in a number of marine fish and argued that it may be used for private communication in an environment devoid of red. Here, we describe the discovery of a chromatophore in fishes that regulates the distribution of fluorescent pigments in parts of the skin. These cells have a dendritic shape and contain motile fluorescent particles. We show experimentally that the fluorescent particles can be aggregated or dispersed through hormonal and nervous control. This is the first description of a stable and natural cytoskeleton-related fluorescence control mechanism in vertebrate cells. Its nervous control supports suggestions that fluorescence could act as a context-dependent signal in some marine fish species and encourages further research in this field. The fluorescent substance is stable under different chemical conditions and shows no discernible bleaching under strong, constant illumination.
PLoS ONE 01/2012; 7(6):e37913. · 3.73 Impact Factor
[show abstract][hide abstract] ABSTRACT: Sex allocation theory predicts that in small mating groups simultaneous hermaphroditism is the optimal form of gender expression. Under these conditions, male allocation is predicted to be very low and overall per-capita reproductive output maximal. This is particularly true for individuals that live in pairs, but monogamy is highly susceptible to cheating by both partners. However, certain conditions favour social monogamy in hermaphrodites. This study addresses the influence of group size on group stability and moulting cycles in singles, pairs, triplets and quartets of the socially monogamous shrimp Lysmata amboinensis, a protandric simultaneous hermaphrodite.
The effect of group size was very strong: Exactly one individual in each triplet and exactly two individuals in each quartet were killed in aggressive interactions, resulting in group sizes of two individuals. All killed individuals had just moulted. No mortality occurred in single and pair treatments. The number of moults in the surviving shrimp increased significantly after changing from triplets and quartets to pairs.
Social monogamy in L. amboinensis is reinforced by aggressive expulsion of supernumerous individuals. We suggest that the high risk of mortality in triplets and quartets results in suppression of moulting in groups larger than two individuals and that the feeding ecology of L. amboinensis favours social monogamy.
Frontiers in Zoology 11/2011; 8:30. · 3.87 Impact Factor
[show abstract][hide abstract] ABSTRACT: Immune responses, either constitutive or induced, are costly. An alternative defence strategy may be based on behavioural responses. For example, avoidance behaviour reduces contact with pathogens and thus the risk of infection as well as the requirement of immune system activation. Similarly, if pathogens are taken up orally, preferential feeding of pathogen-free food may be advantageous. Behavioural defences have been found in many animals, including the nematode Caenorhabditis elegans. We here tested nematodes from a laboratory based evolution experiment which had either coevolved with their microparasite Bacillus thuringiensis (BT) or evolved under control conditions. After 48 generations, coevolved populations were more sensitive to food conditions: in comparison with the controls, they reduced feeding activity in the presence of pathogenic BT strains while at the same time increasing it in the presence of non-pathogenic strains. We conclude that host-parasite coevolution can drive changes in the behavioural responsiveness to bacterial microbes, potentially leading to an increased defence against pathogens.
[show abstract][hide abstract] ABSTRACT: Coevolving hosts and parasites can adapt to their local antagonist. In studies on natural populations, the observation of local adaptation patterns is thus often taken as indirect evidence for coevolution. Based on this approach, coevolution was previously inferred from an overall pattern of either parasite or host local adaptation. Many studies, however, failed to detect such a pattern. One explanation is that the studied system was not subject to coevolution. Alternatively, coevolution occurred, but remained undetected because it took different routes in different populations. In some populations, it is the host that is locally adapted, whereas in others it is the parasite, leading to the absence of an overall local adaptation pattern. Here, we test for overall as well as population-specific patterns of local adaptation using experimentally coevolved populations of the nematode Caenorhabditis elegans and its bacterial microparasite Bacillus thuringiensis. Furthermore, we assessed the importance of random interaction effects using control populations that evolved in the absence of the respective antagonist. Our results demonstrate that experimental coevolution produces distinct local adaptation patterns in different replicate populations, including host, parasite or absence of local adaptation. Our study thus provides experimental evidence of the predictions of the geographical mosaic theory of coevolution, i.e. that the interaction between parasite and host varies across populations.
Proceedings of the Royal Society B: Biological Sciences 02/2011; 278(1719):2832-9. · 5.68 Impact Factor
[show abstract][hide abstract] ABSTRACT: Mating plugs that males place onto the female genital tract are generally assumed to prevent remating with other males. Mating plugs are usually explained as a consequence of male-male competition in multiply mating species. Here, we investigated whether mating plugs also have collateral effects on female fitness. These effects are negative when plugging reduces female mating rate below an optimum. However, plugging may also be positive when plugging prevents excessive forced mating and keeps mating rate closer to a females' optimum. Here, we studied these consequences in the gonochoristic nematode Caenorhabditis remanei. We employed a new CO2-sedation technique to interrupt matings before or after the production of a plug. We then measured mating rate, attractiveness and offspring number.
The presence of a mating plug did not affect mating rate or attractiveness to roving males. Instead, females with mating plugs produced more offspring than females without copulatory plugs.
Our experiment suggests that plugging might have evolved under male-male competition but represents a poor protection against competing males in our experiment. Even if plugging does not reduce mating rate, our results indicate that females may benefit from being plugged in a different sense than remating prevention.
Frontiers in Zoology 11/2010; 7:28. · 3.87 Impact Factor
[show abstract][hide abstract] ABSTRACT: The coevolution between hosts and parasites is predicted to have complex evolutionary consequences for both antagonists, often within short time periods. To date, conclusive experimental support for the predictions is available mainly for microbial host systems, but for only a few multicellular host taxa. We here introduce a model system of experimental coevolution that consists of the multicellular nematode host Caenorhabditis elegans and the microbial parasite Bacillus thuringiensis. We demonstrate that 48 host generations of experimental coevolution under controlled laboratory conditions led to multiple changes in both parasite and host. These changes included increases in the traits of direct relevance to the interaction such as parasite virulence (i.e., host killing rate) and host resistance (i.e., the ability to survive pathogens). Importantly, our results provide evidence of reciprocal effects for several other central predictions of the coevolutionary dynamics, including (i) possible adaptation costs (i.e., reductions in traits related to the reproductive rate, measured in the absence of the antagonist), (ii) rapid genetic changes, and (iii) an overall increase in genetic diversity across time. Possible underlying mechanisms for the genetic effects were found to include increased rates of genetic exchange in the parasite and elevated mutation rates in the host. Taken together, our data provide comprehensive experimental evidence of the consequences of host-parasite coevolution, and thus emphasize the pace and complexity of reciprocal adaptations associated with these antagonistic interactions.
Proceedings of the National Academy of Sciences 04/2010; 107(16):7359-64. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Theory predicts that occasional sexual reproduction in predominantly parthenogenetic organisms offers all the advantages of obligate sexuality without paying its full costs. However, empirical examples identifying and evaluating the costs and benefits of rare sex are scarce. After reviewing the theoretical perspective on rare sex, we present our findings of potential costs and benefits of occasional sex in polyploid, sperm-dependent parthenogens of the planarian flatworm Schmidtea polychroa. Despite costs associated with the production of less fertile tetraploids as sexual intermediates, the benefits of rare sex prevail in S. polychroa and may be sufficiently strong to prevent extinction of parthenogenetic populations. This offers an explanation for the dominance of parthenogenesis in S. polychroa. We discuss the enigmatic question why not all organisms show a mixed reproduction mode.
The Journal of heredity 03/2010; 101 Suppl 1:S34-41. · 2.05 Impact Factor
[show abstract][hide abstract] ABSTRACT: When mating effort (e.g. via ejaculates) is high, males are expected to strategically allocate their resources depending on the expected fitness gains from a given mating opportunity. One mechanism to achieve strategic mating is the Coolidge effect, where male sexual motivation declines across repeated encounters with a familiar partner, but resuscitates when encountering a novel female. Experimental tests of male mate choice via mechanisms such as the Coolidge effect, however, remain scarce. Moreover, it is untested to date whether the Coolidge effect occurs in a sex-specific manner in simultaneous hermaphrodites, where the motivation to mate with a familiar partner may vary with previous mating activity in the male or female role.
We exposed focal hermaphroditic freshwater snails, Biomphalaria glabrata, repeatedly to either a familiar or a novel partner. None of our proxies of sexual motivation (remating likelihood, mating delay, copulation duration) varied between the novel and familiar partner treatments. Moreover, the mating role taken during the first copulation did not affect the subsequent choice of mating roles in the familiar partner treatment as would be expected if focals preferred to avoid mating twice in the same role with a familiar partner. This indicates the absence of sex-specific effects of partner novelty.
Our data indicate that mate novelty does affect neither overall sexual motivation nor the choice of mating roles in B. glabrata. Hence, male mate choice via a Coolidge effect appears inexistent in this invertebrate hermaphrodite. We discuss the possible roles of insufficient fitness gains for discriminatory behaviour in populations with frequent mate encounters as well as poor mate discrimination capacities. Our findings lend also no support to the novel prediction that sexual motivation in simultaneous hermaphrodites varies with the mating roles taken during previous copulations, calling for empirical investigation in further hermaphrodite systems.
Frontiers in Zoology 10/2009; 6:23. · 3.87 Impact Factor
[show abstract][hide abstract] ABSTRACT: Besides their remarkable capability of regeneration, planarian flatworms are well known for their wide range of reproductive
modes. In this chapter, we elucidate the evolutionary significance of sexual and parthenogenetic reproduction in the freshwater
planarian Schmidtea polychroa. In accordance with the major theories of sex, parthenogenetic S. polychroa seem to suffer from both a higher mutation load and parasite load. Nevertheless, parthenogenesis is still maintained in S. polychroa and is more prevalent across Europe than sexual reproduction. The success of parthenogenesis can be explained by occasional
sexual events in predominantly parthenogenetic types. We stress the evolutionary consequences of such rare sexual processes
for the success and maintenance of parthenogenesis. At the end of the chapter, we speculate on what future perspectives this
system still has to offer.
[show abstract][hide abstract] ABSTRACT: Monocystis sp. are sporocyst-forming apicomplexan parasites common in seminal vesicles of the earthworm Lumbricus terrestris where they may account for temporary castration. This study describes the internal transcribed spacer (ITS) region of the ribosomal cistron of Monocystis sp. This region, including ITS-1, the 5.8S ribosomal RNA gene, and ITS-2, was PCR amplified, cloned, and sequenced for Monocystis sp. isolated from the seminal vesicles of several wild-caught L. terrestris. Our analysis revealed substantial polymorphisms, also within single host organisms, indicating intra-host diversity of parasites. These genetic markers are the first that allow distinction of Monocystis sp. genotypes, opening new avenues for the study of parasite diversity within and between hosts.