Female Reproductive Characters Research Articles

Reproductive transitions in plants and animals: selfing syndrome, sexual selection and speciation.

The evolution of predominant self-fertilisation frequently coincides with the evolution of a collection of phenotypes that comprise the 'selfing syndrome', in both plants and animals. Genomic features also display a selfing syndrome. Selfing syndrome traits often involve changes to male and female reproductive characters that were subject to sexual selection and sexual conflict in the obligatorily outcrossing ancestor, including the gametic phase for both plants and animals. Rapid evolution of reproductive traits, due to both relaxed selection and directional selection under the new status of predominant selfing, lays the genetic groundwork for reproductive isolation. Consequently, shifts in sexual selection pressures coupled to transitions to selfing provide a powerful paradigm for investigating the speciation process. Plant and animal studies, however, emphasise distinct selective forces influencing reproductive-mode transitions: genetic transmission advantage to selfing or reproductive assurance outweighing the costs of inbreeding depression vs the costs of males and meiosis. Here, I synthesise links between sexual selection, evolution of selfing and speciation, with particular focus on identifying commonalities and differences between plant and animal systems and pointing to areas warranting further synergy.

Comparison of reproductive investment in native and non‐native populations of common wall lizards reveals sex differences in adaptive potential

Non‐native animals can encounter very different environments than those they are adapted to. Functional changes in morphology, physiology and life‐history following introduction show that organisms can adapt both fast and efficiently. It remains unclear, however, if female reproductive characters and male sexually selected behaviour show the same adaptive potential. Furthermore, the invasion success and evolutionary trajectory of non‐native species might often depend on the ability of the sexes to coordinate shifts in characters associated with reproductive strategy. The common wall lizard, Podarcis muralis, has been repeatedly introduced from southern Europe to England over the past 80 years. Lizards in England experience a cool, seasonal climate that effectively restricts recruitment to the first clutch of the season, whereas in their native range up to three clutches per season recruit. As a consequence, both females and males in non‐native populations should benefit from reducing or even eliminating their reproductive investment in second clutches. Using a combination of field data and experiments, we show that non‐native females produce relatively larger and heavier first seasonal clutches and smaller and lighter second seasonal clutches compared to native females. In contrast, non‐native and native males do not differ in their territorial and sexual behaviour later in the season. An adaptive shift in male seasonal reproductive investment may be constrained because males use breeding females as cues for sexual behaviour. If this is so, we expect a general pattern across climatic regimes whereby female reproductive investment evolves first, with responses in males lagging behind.

Molecular and morphological circumscription ofMesocestoidestapeworms from red foxes (Vulpes vulpes) in central Europe

Here we examine 3157 foxes from 6 districts of the Slovak Republic in order to determine for the first time the distribution, prevalence and identity of Mesocestodes spp. endemic to this part of central Europe. During the period 2001-2006, an average of 41.9% of foxes were found to harbour Mesocestoides infections. Among the samples we confirmed the widespread and common occurrence of M. litteratus (Batsch, 1786), and report the presence, for the first time, of M. lineatus (Goeze, 1782) in the Slovak Republic, where it has a more restricted geographical range and low prevalence (7%). Using a combination of 12S rDNA, CO1 and ND1 mitochondrial gene sequences together with analysis of 13 morphometric characters, we show that the two species are genetically distinct and can be differentiated by discrete breaks in the ranges of the male and female reproductive characters, but not by the more commonly examined characters of the scolex and strobila. Estimates of interspecific divergence within Mesocestoides ranged from 9 to 18%, whereas intraspecific variation was less than 2%, and phylogenetic analyses of the data showed that despite overlapping geographical ranges, the two commonly reported European species are not closely related, with M. litteratus more closely allied to North American isolates of Mesocestoides than to M. lineatus. We confirm that morphological analysis of reproductive organs can be used to reliably discriminate between these often sympatric species obtained from red foxes.

Co‐evolution of male and female reproductive traits across the Bruchidae (Coleoptera)

1. Despite the obvious importance of spermatozoa to individual reproductive success a general explanation of variation in spermatozoan form and function is still lacking. In species with internal fertilization, sperm not only have to interact with the physical and biochemical environment of the female reproductive tract, but frequently face competition from the sperm of rival males. Both sperm competition theory and adaptation to the selective environment of the female reproductive tract have been implicated in the evolution of spermatozoan morphological diversity. 2. Using the comparative method, we examine variation in sperm length in relation to (i) sperm competition intensity (as measured by relative testis size) and (ii) female reproductive characters, across 15 species of beetle belonging to the family Bruchidae. 3. Stepwise multiple regression within a phylogenetic framework revealed sperm length to be positively correlated with female spermathecal duct length and negatively related to spermathecal volume, but not testes size, indicating that the female reproductive environment rather than sperm competition per se exerts selection on sperm length in this taxonomic group. 4. A positive association between testes volume and the volume of the female spermatheca was also evident suggesting correlated evolution of these traits. 5. A number of models of sexual selection could lead to the correlated evolution of male and female reproductive characters, although the underlying mechanisms of cause and effect remain elusive. Divergence between species (and populations) in primary reproductive traits is likely to present a significant barrier to hetero-specific fertilization, and thus contribute to reproductive isolation.

ASSESSING THE POTENTIAL FOR AN ONGOING ARMS RACE WITHIN AND BETWEEN THE SEXES: SELECTION AND HERITABLE VARIATION

In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on one's mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.

Genetic Variation in Male and Female Reproductive Characters Associated with Sexual Conflict in Drosophila melanogaster

Recent studies have shown that elevated mating, courtship and seminal substances affect female fitness negatively in Drosophila melanogaster. It has also been shown that males vary with respect to these characters and that male harm to females correlates positively with components of male fitness. These results suggest that there is sexual conflict over the effect of such male characters. An important component of this scenario is that females have evolved counteradaptations to male harm, but so far there is limited evidence for this. Here I define female resistance as the ability to withstand an increased exposure to males. Across 10 genetically differentiated lines of D. melanogaster, I found genetic variation among females in the reduction of lifespan that followed from exposure to males of different durations. There was also genetic variation among males with regards to the degree to which they decrease the lifespan of their mates. These results suggest that genetic variation for female ability to endure male sexually antagonistic adaptations exists and may play an important role in male-female coevolution.

Co‐evolution of male and female reproductive characters across the Scathophagidae (Diptera)

Sperm morphometry is extremely variable across species, but a general adaptive explanation for this diversity is lacking. As sperm must function within the female, variation in sperm form may be associated with variation in female reproductive tract morphology. We investigated this and other potential evolutionary associations between male and female reproductive characters across the Scathophagidae. Sperm length was positively associated with the length of the spermathecal (sperm store) ducts, indicating correlated evolution between the two. No association was found between sperm length and spermathecal size. However, the size of the spermathecae was positively associated with testis size indicating co-evolution between male investment in sperm production and female sperm storage capacity. Furthermore, species with a higher degree of polyandry (larger testes) had longer spermathecal ducts. However, no associations between sperm length or length variation and testis size were found which suggests greater sperm competition sensu stricto does not select for longer sperm.

ASSESSING THE POTENTIAL FOR AN ONGOING ARMS RACE WITHIN AND BETWEEN THE SEXES: SELECTION AND HERITABLE VARIATION

In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on one's mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.

Disruptive selection on female reproductive characters in a hybrid zone of Littorina saxatilis

We studied natural selection in a hybrid zone of the intertidal marine snail Littorina saxatilis located in Galicia (NW Spain) by measuring the number and average size of the embryos carried by females. We related these characters with the females' position on the phenotypic and environmental gradients between the two pure morphs of the hybrid zone. In contrast with previous interpretations of studies made in this hybrid zone, we found a depression in both embryo number and size for phenotypically intermediate females. This disruptive natural selection could play an important role in the maintenance of the population's bimodal phenotypic distribution and in that of the assortative mating between the pure morphs. We found also that intermediate environments tended to be unfavorable for all phenotypes. Although the precise causes for the found depression in female reproductive characters remain to be determined, these results serve to emphasize the importance of studying whole fitness surfaces in hybrid zones, across the complete phenotypic and environmental ranges, instead of merely comparing the fitness averages of the two pure morphs and the intermediate individuals, taken as three discrete phenotypic classes.

Sexual conflict selects for male and female reproductive characters

Background: Strict genetic monogamy leads to sexual harmony because any trait that decreases the fitness of one sex also decreases the fitness of the other. Any deviation from monogamy increases the potential for sexual conflict. Conflict is further enhanced by sperm competition, and given the ubiquity of this phenomenon, sexual conflict is rife. In support of theory, experimentally enforced monogamy leads to the evolution of sexual benevolence. In contrast, with multiple mating, males evolve traits causing massive female fitness reductions when female evolution is restrained. Theory also predicts increased investment in spermatogenesis when sperm competition risk is high. While this supposition has correlational support, cause and effect has yet to be firmly established.Results: By enforcing monogamy or polyandry in yellow-dung-fly lines, we have shown experimentally that males from polyandrous treatments evolved larger testes. Furthermore, females from this treatment evolved larger accessory sex glands. These glands produce a spermicidal secretion, so larger glands could increase female ability to influence paternity. Using molecular techniques, we have shown that, consistent with this idea, males' success as second mates is reduced in females from the polyandrous treatment. Nevertheless, males from polyandrous lines achieve higher paternity during sperm competition, and this finding further supports the testis evolution patterns.Conclusions: These results provide direct experimental support for macroevolutionary patterns of testis size evolution. Furthermore, we have shown that sperm competition selects for traits likely to be important in sexual conflicts over paternity, a result only previously demonstrated in Drosophila melanogaster.

The evolution of sperm length in moths.

Sperm form and function remain poorly understood despite being of fundamental biological importance. An instructive approach has been to examine evolutionary associations across comparable taxa between sperm characters and other, potentially selective reproductive traits. We adopt this approach here in a comparative study examining how sperm lengths are associated with male and female reproductive characters across moths. Primary data have revealed Lepidoptera to be an ideal order for examination: there is profound variation in the dimensions (but not organization) of the reproductive traits between closely related species which all share a monophyletic ancestry, for example, eupyrene sperm length varies from 110 to 12,675 microm. Eupyrene (normal fertilizing) and apyrene (anucleate and non-fertile) sperm lengths are positively correlated across taxa and both sperm types show positive associations with mating pattern (as measured by the residual testis size). At fertilization, eupyrene sperm must migrate down the often elongated female spermathecal duct from storage to unite with the ovum. Across taxa, the elongation of this duct is associated with increased eupyrene sperm length, suggesting a positive female influence on sperm size since longer, more powerful sperm may be selected to migrate and/or compete successfully down greater ductal lengths. Apyrene sperm length is not associated with female reproductive tract dimensions. However, we found a positive relationship between the residual testis volume and spermathecal volume, suggesting coevolution between male investment in spermatogenesis and the extent of the female sperm storage capacity. Within males, there is a positive association between the two organs which form the ejaculate-containing spermatophore: the testes and the accessory gland. The 'trade-up' in investment to these components is discussed in relation to paternal investment and mating patterns.

EFFECTS OF FOLIAR HERBIVORY ON MALE AND FEMALE REPRODUCTIVE TRAITS OF WILD RADISH,RAPHANUS RAPHANISTRUM

In this study, we examined how foliar herbivory affected the relative allo- cation to male and female reproductive traits in a hermaphroditic plant. In two experiments, one in the greenhouse and the other in a growth chamber, leaves of full sibling plants of the annual wild radish, Raphanus raphanistrum, received one of four damage treatments to leaves (0, 25% (two types), or 50% leaf area removal). We controlled natural damage by Pieris rapae larvae through the use of clip cages. Measurements of both male and female reproductive characters were made on a series of flowers produced by each plant over its lifetime. We measured pollen production, pollen size, ovule number, ovule size, petal size, nectar production, and sugar content. Effects of herbivory on plant phenology were also assessed. At the end of the experiment, we quantified total flower production, fruit pro- duction, number of seeds and fruit, and seed and vegetative biomass. In general, male reproductive characters were more affected than female characters by herbivory. Leaf herbivory reduced pollen number and pollen size, whereas ovule size and number were not affected. Petal size, which we also classify more as a male trait, decreased with herbivory. Plants were generally able to completely compensate for herbivory in the total number of flowers and fruit they produced; however, fewer fruits were found in the heaviest damage treatment in the growth chamber experiment. We discuss alternative ex- planations for this pattern based on developmental constraints and adaptive responses. In summary, male fitness traits were much more strongly affected by herbivory than were female traits; full compensation in seed production after herbivory may come at the cost of male reproductive success in these hermaphroditic plants.

Snail sperm production characteristics vary with sperm competition risk

Sperm competition is widespread and influences both male investment in spermatogenic tissue and ejaculate characteristics. Sperm competition models assume trade-offs between sperm size and number, although such trade-offs may be difficult to detect. This study examines the effects of sperm competition risk on the sperm production characteristics of the freshwater snail Viviparus ater. In this prosobranch, females mate frequently and store sperm, generating sperm competition. Males produce two sperm morphs, fertile eupyrene sperm and non-fertilizing oligopyrene sperm. Non-fertilizing sperm may play a role in sperm competition and therefore, like fertilizing sperm, the number produced could vary relative to sperm competition risk. In addition, trade-offs between sperm number and sperm size may be expected. We manipulated the sex ratio of sexually mature snails and found the presence of rivals affected the ratio of oligopyrene/eupyrene sperm males produced. In experimental and natural populations, the number of oligopyrene sperm produced, but not the number of eupyrene sperm, was significantly higher when the sex ratio was male biased. Testis mass did not vary between experimental treatments. We also found a negative relationship between the number and size of oligopyrene sperm produced, which is consistent with evolutionary models of sperm competition, and is, to our knowledge, the first intraspecific demonstration of a trade-off between these traits.

Phylogeny, Molecules Versus Morphology, and Rates of Character Evolution Among Fruitbats (Chiroptera: Megachiroptera)

Andersen's 1912 monograph on megachiropterans remains the definitive work on the systematics of this group. Andersen argued that the Macroglossinae, containing the eonycterine and notopterine sections, are a monophyletic sister-group to other fruitbats (i.e. Andersen's Rousettus, Cynopterus and Epomophorus sections). Two recent molecular studies (DNA hybridisation and restriction mapping of ribosomal cistrons), as well as an analysis of female reproductive characters, challenge the monophyly of the Macroglossinae and several of Andersen's other conclusions such as the phylogenetic position of Nyctimene. We performed a cladistic analysis on 36 morphological characters, including 33 that were gleaned from Andersen, to determine whether phylogenetic hypotheses based on modem phylogenetic methods are in agreement with Andersen's original conclusions and to compare morphological and molecular phylogenetic hypotheses. Minimum-length trees based on parsimony are largely consistent with Andersen and support (1) a monophyletic Macroglossinae, within which the eonycterine section is paraphyletic with respect to a monophyletic notopterine section, (2) a monophyletic Cynopterus section, excepting the exclusion of Myonycteris, (3) a monophyletic Epomophorus section, excepting the exclusion of Plerotes, and (4) a paraphyletic Rousettus section, with several of the Rousettus-like forms branching off near the base of the tree. Bootstrapping analyses on a reduced data-set that included taxa shared in common with the DNA hybridisation study did not provide strong support (greater than or equal to 95%) for any clades but did provide moderate support (greater than or equal to 70) for several clades, including a monophyletic Macroglossinae. These findings are in marked contrast to the DNA hybridisation phylogeny. A high index of between-data-set incongruence is further evidence for the clash between DNA hybridisation and morphology. A phylogenetic framework was constructed on the basis of morphological data and DNA hybridisation data using a criterion of moderate support and shows little resolution, whereas employing a criterion of strong support produced a framework resolving several additional nodes. One implication of this framework is that characteristic macroglossine features such as a long tongue with a thick carpet of filiform papillae have evolved independently on several occasions (or evolved once and were lost several times). Rates of character evolution for the morphological characters employed in our analysis were calculated using divergence times estimated from DNA hybridisation data. Rates have apparently been fastest in the interior branches, and slower along the external branches, which suggests an early adaptive radiation in the history of fruitbats.

Genetic Constraints on the Independent Evolution of Male and Female Reproductive Characters in the Tristylous Plant Lythrum salicaria

Genetic Constraints on the Independent Evolution of Male and Female Reproductive Characters in the Tristylous Plant Lythrum salicaria

Estimates of hierarchical variation in flower morphology in natural populations ofScleranthus annuus (Caryophyllaceae), an inbreeding annual

The variation in two sets of morphological characters of the flowers of the highly inbreedingScleranthus annuus (Caryophyllaceae) was assessed using 15–20 plants from each of 20 natural populations from the southernmost region of Sweden. The stamen fertility data set consisted of 10 characters describing the degree of fertility of the ten stamens/staminoids, while the sepal/gynoecium data set comprised 10 sepal characters, together with style and stigma length. Substantial variation was found in both the degree of development and the fertility of the stamens, the degree of variability in stamen fertility being related to stamen position within the flower. Considerable variation was found in the characters of the sepal and the gynoecium. Hierarchical analyses of variance indicated that 29% of the variation in total male reproductive effort was distributed among populations, 28% among plants within populations and 43% represented within-plant variation. The corresponding averages for the characters from the sepal/gynoecium data set are 26, 38, and 35%: a greater proportion of the total variance in female reproductive characters is accounted for by among individual variation than is the case with the male reproductive characters. Significance tests of Mahalanobis’ distances derived by canonical variate analyses indicated that all populations were significantly separated using the sepal/gynoecium data set, while only 50% of the pairwise comparisons on the basis of the stamen fertility data set were significant. Cluster analysis did not reveal any aggregation of the populations. The incongruence of the two data sets and their ability to discriminate between the populations is discussed.