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Mating behaviour in Schistosomes: are paired worms always faithful?

Previously assumed to be monogamous, the mating system of schistosomes has been the subject of some debate since recent findings have shown that change of mate can occur among these parasites. Here, Louis-Albert Tchuem Tchuenté, Vaughan R. Southgate, Claude Combes and Joseph Jourdane review progress made in the understanding of the mating behaviour of schistosomes, and highlight the importance of mating systems in the dynamics of natural transmission of schistosomiasis.

Journal Article↗

Evolution of plant breeding systems.

Breeding systems are important, and often neglected, aspects of the natural biology of organisms, affecting homozygosity and thus many aspects of their biology, including levels and patterns of genetic diversity and genome evolution. Among the different plant mating systems, it is useful to distinguish two types of systems: 'sex systems', hermaphroditic versus male/female and other situations; and the 'mating systems' of hermaphroditic populations, inbreeding, outcrossing or intermediate. Evolutionary changes in breeding systems occur between closely related species, and some changes occur more often than others. Understanding why such changes occur requires combined genetical and ecological approaches. I review the ideas of some of the most important theoretical models, showing how these are based on individual selection using genetic principles to ask whether alleles affecting plants' outcrossing rates or sex morphs will spread in populations. After discussing how the conclusions are affected by some of the many relevant ecological factors, I relate these theoretical ideas to empirical data from some of the many recent breeding system studies in plant populations.

Biological Evolution↗

A spatially explicit individual-based model of reinforcement in hybrid zones.

An individual-based model consisting of two dioecious populations in a two-dimensional environmental grid was constructed. Each population began with, and never exceeded, 1000 individuals; extinction was allowed. Genomes consisting of 30 biallelic loci for male sexual advertisement call, female mate preference, and population origin were constructed, and lineages of each individual in the starting populations were followed for 2000 generations. Type and level of hybrid disadvantage, initial population distribution, patchiness of environmental resources, and level of mate choice were varied. Persistence of bimodal hybrid zones was nonexistent at low levels of hybrid disadvantage and universal at high levels of hybrid disadvantage, with a narrow threshold in which persistence was unpredictable. Persistence occurred at lower levels of hybrid disadvantage when populations were initially parapatric rather than sympatric, and environments were patchy rather than homogeneous. Increased divergence in mating systems occurred when hybrid disadvantage was high, hybrids were infertile, populations were initially parapatric, and increased female choice was allowed. Mating system divergence was much higher in interacting populations compared with noninteracting populations, indicating that reinforcement caused most of the observed divergence. When hybrids were infertile, reinforcement contributed to speciation, because under hybrid infertility the probability of persistence at low levels of hybrid disadvantage was positively related to mate choice. The results agree with previous one-dimensional spatial models in finding that population persistence is more likely in parapatric and patchy population distributions. In addition, the results show that hybrid infertility may facilitate the process of reinforcement and speciation.

Biological Evolution↗

Fine-scale estimation of outcrossing in western redcedar with microsatellite assay of bulked DNA.

Western redcedar (Thuja plicata, Cupressaceae) is a self-fertile conifer with a mixed mating system and significant variation for outcrossing among populations. In this paper, we conducted a fine-scale study of mating system variation to identify correlates of outcrossing in natural populations. We examined variation for outcrossing within and among individual trees, and describe a new method to estimate outcrossing using bulked DNA samples. Bulking (assaying DNA tissues from several individuals simultaneously) increases the experimental power without increasing the experimental effort. We sampled 80 trees from four natural populations in southwestern British Columbia. From each tree, we sampled from up to six crown positions (three heights and inner vs outer branches). From each position, two samples of three seedlings each were bulked before DNA extractions. Using four microsatellite loci, we obtained outcrossing rates for each tree and for each of the six crown positions. We found individual tree selfing rates to increase with tree height in all four populations, but selfing rates did not differ among crown positions. The higher selfing rate of larger trees is probably due to their greater proportional contribution to local pollen clouds. Individual tree outcrossing rates ranged from 22 to 100% and the population outcrossing rates from 66 to 78%. Missed alleles due to bulking and the estimation method used both cause a downward bias in outcrossing rates, so that these estimates are probably lower than the actual outcrossing rates. Nevertheless, the trends we observed are not affected by systematic biases of estimation.

Cedrus↗

The cost of fluctuating inbreeding depression.

We present a phenotypic model for the evolution of self-fertilization in an infinite population of annual hermaphrodites for the case in which fitness and inbreeding depression vary among generations (e.g., due to fluctuations in the environment from year to year). Conditions for the evolution of selfing, mixed mating, and outcrossing are derived and are compared with results from numerical calculations that assume a normal distribution of inbreeding depression. In contrast to the situation in which inbreeding depression does not vary, when inbreeding depression fluctuates in a stochastic manner among generations with a mean less than 0.5, selfing is not necessarily selected. Thus, fluctuating inbreeding depression can be viewed as an additional cost of selfing that may stabilize mixed mating systems. These results emphasize the need to take into account fluctuating inbreeding depression in empirical studies aimed at understanding mating system evolution in annuals.

Biological Evolution↗

Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations.

The fact that selfing increases seed set (reproductive assurance) has often been put forward as an important selective force for the evolution of selfing. However, the role of reproductive assurance in hermaphroditic populations is far from being clear because of a lack of theoretical work. Here, I propose a theoretical model that analyzes self-fertilization in the presence of reproductive assurance. Because reproductive assurance directly influences the per capita growth rate, I developed an explicit demographic model for partial selfers in the presence of reproductive assurance, specifically when outcrossing is limited by the possibility of pollen transfer (Allee effect). Mating system parameters are derived as a function of the underlying demographical parameters. The functional link between population demography and mating system parameters (reproductive assurance, selfing rate) can be characterized. The demographic model permits the analysis of the evolution of self-fertilization in stable populations when reproductive assurance occurs. The model reveals some counterintuitive results such as the fact that increasing the fraction of selfed ovules can, in certain circumstances, increase the fraction of outcrossed ovules. Moreover, I demonstrate that reproductive assurance per se cannot account for the evolution of stable mixed selfing rates. Also, the model reveals that the extinction of outcrossing populations depends on small changes in population density (ecological perturbations), while the transition from outcrossing to selfing can, in certain cases, lead the population to extinction (evolutionary suicide). More generally, this paper highlights the fact that self-fertilization affects both the dynamics of individuals and the dynamics of selfing genes in hermaphroditic populations.

Biological Evolution↗

Genetic selection strategies: computer modeling.

There are four primary factors to consider in genetic selection strategies: 1) accuracy of selection, 2) selection intensity, 3) effective population size, and 4) mating system. Current theory indicates that optimum response to selection is achieved by maximizing the first three factors and using a mating systems that allows optimization of reproductive characteristics in dam lines and production characteristics in sire lines. However, with limited resources, compromises among the first three factors are needed. Simulations are useful for examining those compromises. Unrealistic simplifying assumptions are necessary for analytic theoretical results and thus do not address real world breeding problems. Using simulations, the relationship between selection accuracy, which is increased by use of family selection indices or Best Linear Unbiased Prediction (BLUP), and response to selection was examined. Results show that those procedures place a great restriction on effective population size, which offsets most of their advantage, i.e., there is too little emphasis on effective population size. A revision of the methodology and a reappraisal of the results of selection theory for optimization of genetic response is required. Another relationship that is of fundamental importance in breeding programs is that between selection intensity and effective population size. Analytical results for the additive case have been developed but have never been extended to heterotic traits. A gene level simulation program was developed to examine that relationship. Results show that the optimal selection strategy depends on the trait being selected. For additive traits and in the short term (20 generations), one should maximize selection intensity. For heterotic traits, an intermediate proportion (25% of each sex) gives optimal response. In all breeding strategies, primary attention must be given to the rate of inbreeding, which is increased by increasing either accuracy of selection or selection intensity. Inbreeding reduces response to selection in two ways. First, for both additive and nonadditive traits, inbreeding is a measure of the amount of random genetic drift that has occurred. Genetic drift causes loss of favorable alleles. Once lost, those alleles can never be recovered and thus genetic drift lowers the selection limit. Second, for heterotic traits, inbreeding results in a depression of the mean caused by directional dominance.

Animals↗

Evolution of sexual asymmetry.

BACKGROUND: The clear dominance of two-gender sex in recent species is a notorious puzzle of evolutionary theory. It has at least two layers: besides the most fundamental and challenging question why sex exists at all, the other part of the problem is equally perplexing but much less studied. Why do most sexual organisms use a binary mating system? Even if sex confers an evolutionary advantage (through whatever genetic mechanism), why does it manifest that advantage in two, and exactly two, genders (or mating types)? Why not just one, and why not more than two? RESULTS: Assuming that sex carries an inherent fitness advantage over pure clonal multiplication, we attempt to give a feasible solution to the problem of the evolution of dimorphic sexual asymmetry as opposed to monomorphic symmetry by using a spatial (cellular automaton) model and its non-spatial (mean-field) approximation. Based on a comparison of the spatial model to the mean-field approximation we suggest that spatial population structure must have played a significant role in the evolution of mating types, due to the largely clonal (self-aggregated) spatial distribution of gamete types, which is plausible in aquatic habitats for physical reasons, and appears to facilitate the evolution of a binary mating system. CONCLUSIONS: Under broad ecological and genetic conditions the cellular automaton predicts selective removal from the population of supposedly primitive gametes that are able to mate with their own type, whereas the non-spatial model admits coexistence of the primitive type and the mating types. Thus we offer a basically ecological solution to a theoretical problem that earlier models based on random gamete encounters had failed to resolve.

Animals↗

[Fertility of male Syrian hamsters paired with one, two and four proestrous females each].

In order to improve the productivity of Syrian hamsters, we investigated whether a male could impregnate overnight more than one proestrous female. Twenty-one males and 49 females aged 8 to 10 weeks were used in this experiment. The mating systems were as follows: one male was paired with one female, one male was paired with two females, and one male was paired with four females. Six out of 7, 7 of 14 and 4 of 28 females became pregnant and gave birth under these three systems, respectively. We conclude that it is possible for a male to impregnate overnight about one female under the above mating systems.

Animals↗

Habitat age, breeding system and kinship in the ant Formica fusca.

In polygyne ants (multiple queens per colony) factors that affect the distribution and survival of queens may play a key role in shaping the population-wide mating system and colony kin structure. The aim of this paper was to study the breeding system in two populations of different age in the facultatively polygyne ant Formica fusca. Both the observed numbers of queens, and the relatedness patterns among queens, workers and colony fathers were compared in two adjacent populations (ages 17 years and > 100 years) in Southern Finland. The results showed that both the mating system and colony kin structure differed between the study populations. In the old population the relatedness among workers, queens and colony fathers was high. The queens were also related to their mates, resulting in significant inbreeding in workers, but not in queens. Finally, the number of queens per colony fluctuated between years, suggesting queen turnover, and nest-mate queens shared their reproduction unequally (reproductive skew). In the younger population relatedness among queens and workers was lower than in the old population, and the colony fathers were unrelated. Furthermore, inbreeding was absent, and no conclusive evidence was found for reproductive skew among nest-mate queens. Finally, the number of queens per colony appeared more stable between years, although queen turnover occurred also in this population. The observed differences in dispersal and mating behaviour are discussed in the light of a potential connection between population age and habitat saturation.

Age Factors↗

To self, or not to self... a review of outcrossing and pollen-mediated gene flow in neotropical trees.

Despite the typically low population densities and animal-mediated pollination of tropical forest trees, outcrossing and long-distance pollen dispersal are the norm. We reviewed the genetic literature on mating systems and pollen dispersal for neotropical trees to identify the ecological and phylogenetic correlates. The 36 studies surveyed found >90% outcrossed mating for 45 hermaphroditic or monoecious species. Self-fertilization rates varied inversely with population density and showed phylogenetic and geographic trends. The few direct measures of pollen flow (N=11 studies) suggest that pollen dispersal is widespread among low-density tropical trees, ranging from a mean of 200 m to over 19 km for species pollinated by small insects or bats. Future research needs to examine (1) the effect of inbreeding depression on observed outcrossing rates, (2) pollen dispersal in a wide range of pollination syndromes and ecological classes, (3) and the range of variation of mating system expression at different hierarchical levels, including individual, seasonal, population, ecological, landscape and range wide.

Genetic Markers↗

Role of sexual and natural selection in evolution of body size and shape: a phylogenetic study of morphological radiation in grouse.

We use standardized independent contrasts (SICs) to elucidate the effect of ecology and mating systems on morphological radiation in grouse. The analysis of SICs for 38 skeletal measurements from 20 taxa, showed that changes in mating system had a significant effect on body size of both sexes. Sexual size dimorphism in grouse is consistent with Rensch's rule; the slope of the regression of male vs. female size SICs was 1.4, significantly >1. Changes in habitat were associated with accelerated rates of evolution of body proportions. SICs for male and female scores of size independent factors were directly proportional to each other (slope = 1), indicating extreme similarities between male and female ecology. Females, however, were better adapted to longer, more energy efficient flight than males. Size independent morphological differences among grouse are adaptive and are related to the differences in habitat and foraging behaviour among the species.

Animals↗

Larval growth, juvenile size and heterozygosity in laboratory reared mussels, Mytilus edulis.

Studies with marine bivalve juveniles have shown a positive correlation between growth and allozyme multi-locus heterozygosity (MLH), and, in some cases, between larval growth and juvenile growth, but there has been little research on the relationship between allozyme heterozygosity and larval growth. Larvae of M. edulis from different mating systems (half-sib families with a single female, or a single male parent, a reciprocal cross of two malesxtwo females and two mass matings of 13x13 and 8x17 females and males, respectively) were reared in the laboratory and selected into fast and slow growing groups when about 10-30% were undergoing metamorphosis. Offspring were reared to the juvenile stage (>3.00 mm) and both groups of each mating were electrophoresed and genotyped at up to 12 allozyme loci. There was generally good agreement with Mendelian inheritance (half-sibs and reciprocal cross) or the Hardy-Weinberg model (mass matings). Null alleles were detected at the Odh and Lap loci but there was no evidence that null allele heterozygotes grew slower than other genotypes. Over all cohorts, juveniles from the fast growing larval group were not significantly larger, or smaller, than juveniles from the slow growing group which suggests that larval growth rate may be independent of juvenile growth rate. This observation agrees with some, but not all, earlier studies and has commercial relevance. Tests of heterozygosity and juvenile shell length indicated no association between average heterozygosity across all allozyme loci and the size of juveniles in any cohort regardless of the mating system used or their larval growth rate. The association between MLH and juvenile growth in bivalves is seldom detected in cohorts from a limited genetic background. The lack of an association between heterozygosity and size might therefore be expected in the half-sib and reciprocal cross cohorts, but not in the mass matings. The results argue against any significant association between heterozygosity and larval size in mussels.

Journal Article↗

Culture and courtship in vertebrates: a review of social learning and transmission of courtship systems and mating patterns.

Female and male animals often choose mates based upon the complementarity of their courtship behaviours and preferences. The importance of this fact on the evolutionary dynamics of populations has long been appreciated. What has not been appreciated is the role that social learning might play in the transmission of systems of courtship behaviour across generations. This paper addresses the social transmission of courtship behavioural traditions in vertebrates. It discusses views of culture in the context of behavioural signals and preferences in courtship. It then reviews empirical evidence for culture-like processes affecting courtship behaviour, focusing on studies of song learning in passerine birds and work on social learning of mating preferences. The paper concludes with potential future directions for research on social traditions in systems of courtship behaviour, including determining mechanisms of transmission, genetic and non-social environmental effects, and selective factors influencing the stability of behavioural traditions over time. By integrating proximate and ultimate questions for the transmission of courtship systems, this work would increase our understanding of the ways individual development, cultural processes, and population evolution influence, and are in turn influenced by, one another.

Journal Article↗

Sexual selection promotes hybridization between Pecos pupfish, Cyprinodon pecosensis and sheepshead minnow, C. variegatus.

Rapid and extensive genetic introgression has occurred between Pecos pupfish (Cyprinodon pecosensis) and sheepshead minnow (Cyprinodon variegatus) in the wild. We studied both female mate choice and male-male competition for mates among C. pecosensis, C. variegatus, and their F1 hybrids to determine what role these behaviours played in the formation of the hybrid swarm. Female C. pecosensis preferred male C. variegatus to conspecific males, C. variegatus females displayed no significant preference when given a choice between purebred males, and neither C. pecosensis nor C. variegatus females discriminated against F1 hybrid males. We found no evidence for female olfactory recognition of mates. Male F1 hybrids and C. variegatus were more aggressive than C. pecosensis males, achieving greater reproductive success under two different experimentally-induced mating systems. Hybrids were superior to C. variegatus when only two males competed (dominance interactions), but the two types were competitively equivalent in a territorial mating system. Our results indicate that active inter- and intra-sexual selection contributed to the accelerated hybridization between these two species. By including the possibility that some aspects of a hybridization and introgression event may be under positive selection, researchers may better understand the dynamics that lead to hybrid zone stability or the spread of introgressed genetic material.

Aggression↗

Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris.

Outcrossing rate, the rates of ovule and seed abortion, and levels of correlated paternity were estimated in a small population of Pinus sylvestris, a predominantly outcrossing conifer, and were compared with estimates from two widely dispersed woodlands of the same species, showing a range of densities. On average, seed trees of the small population showed an eight-fold higher selfing rate (25 vs. 3%) and a 100-fold greater incidence of correlated paternity (19.6 vs. 0.2%) than did trees from the large populations. No evidence was found of pollen limitation within the remnant stand, as suggested by ovule abortion rates. Investigation of the mating patterns in the small population, based on the unambiguous genealogy of 778 open-pollinated seeds, showed a large departure from random mating. Only 8% of the possible mating pairs within the stand were observed. Correlated paternity rate within a maternal sibship was negatively associated (rs = -0.398, P < 0.050) with the distance to the nearest neighbour, and shared paternity among maternal sibships was negatively correlated (rs = -0.704, P < 0.001) with the distance between seed trees. Numerical simulations, based on the estimated individual pollen dispersal kernel, suggest that restricted dispersal might have been the key factor affecting mating patterns in the small population and, together with low population density, may account for the observed mating system variation between the small and the large populations. The results of this study show that a severe size reduction may substantially affect the mating system of a wind-pollinated, typically outcrossed plant species.

Computer Simulation↗

Reinforcement of genetic coherence: a single-locus model.

Genetic coherence and genetic separation are the outcome of evolutionary mechanisms which maintain genetic variation within populations through recombination on the one hand, and which divide this variation via speciation between reproductively (recombinatorically) more or less isolated populations on the other. While mechanisms of speciation have received considerable attention in biology, their counterpart, mechanisms of genetic coherence, are addressed only implicitly, if at all. Usually, genetic coherence is intuitively associated with the forces maintaining genetic polymorphisms and thus potential for flexible adaptational reaction of populations. However, so far no models seem to exist which explain the evolution of genetic coherence as the natural counterpart of genetic separation or speciation. In this paper a single-locus model is analyzed, in which a mutant allele is introduced into a resident stable diallelic polymorphism, and where this allele is equivalent to one of the resident alleles in all respects with the exception of mating relations. The conditions for replacement of the resident allele by its selectively equivalent mutant are obtained with reference to the associated mating relations. It turned out that for heterozygote advantage the mutant replaces the selectively equivalent resident allele if it increases the mating preferences for carriers of other alleles. The evolution of lower such preferences requires heterozygote inferiority, which confirms the Wallace effect of speciation (by reinforcement). It is argued that this observation suggests that non-selective constituents of the mating system form the section of the genetic system that is responsible for moderating the genetic load implied by adapting selection while simultaneously securing the adaptational potential embodied in the resident allelic variation. Mating systems thus serve the preservation of adaptability.

Adaptation, Physiological↗

Use of DNA fingerprinting to determine parentage in muskrats (Ondatra zibethicus).

The detection of high levels of genetic variability by DNA fingerprinting probes has allowed researchers to accurately assess relatedness. Multiple-mating strategies are characteristic of the mating systems of small mammals. As such, techniques that provide an accurate indication of how individuals are related genetically is of great importance to assess the mating system of a species. In this study, we applied the DNA fingerprinting technique to captive and wild muskrats (Ondatra zibethicus) to determine its usefulness for parentage analysis in wild populations. We found that DNA digested with the restriction enzyme Hae III and probed with Jeffrey's minisatellite 33. 15 identified a large amount of polymorphism in both groups of muskrats. The DNA fingerprinting technique correctly assessed parentage within the captive group. In the wild population, paternity was assigned between two adult males based on diagnostic fragments and similarity of banding patterns. The likelihood that paternity could be misassigned to a full sibling was high in this free-ranging population. However, because natal dispersal in muskrats is male biased, it is unlikely that two brothers would associate with the same female.

Animals↗