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1.
J Evol Biol ; 25(8): 1555-63, 2012 Aug.
Article in English | MEDLINE | ID: mdl-22587227

ABSTRACT

In polyandrous mating systems, male fitness depends on success in premating, post-copulatory and offspring viability episodes of selection. We tracked male success across all of these episodes simultaneously, using transgenic Drosophila melanogaster with ubiquitously expressed green fluorescent protein (i.e. GFP) in a series of competitive and noncompetitive matings. This approach permitted us to track paternity-specific viability over all life stages and to distinguish true competitive fertilization success from differential early offspring viability. Relationships between episodes of selection were generally not present when paternity was measured in eggs; however, positive correlations between sperm competitive success and offspring viability became significant when paternity was measured in adult offspring. Additionally, we found a significant male × female interaction on hatching success and a lack of repeatability of offspring viability across a focal male's matings, which may underlay the limited number of correlations found between episodes of selection.


Subject(s)
Drosophila melanogaster/physiology , Sexual Behavior, Animal/physiology , Animals , Animals, Genetically Modified , Drosophila melanogaster/genetics , Female , Male , Reproduction/physiology , Survival Analysis
2.
J Theor Biol ; 264(3): 1003-23, 2010 Jun 07.
Article in English | MEDLINE | ID: mdl-20206187

ABSTRACT

We examine models for evolution of sperm size (i.e. mass m) and number (s) under three mechanisms of sperm competition at low 'risk' levels: (i) raffle with no constraint on space available for competing sperm, (ii) direct displacement mainly by seminal fluid, and (iii) direct displacement mainly by sperm mass. Increasing sperm mass increases a sperm's 'competitive weight' against rival sperm through a diminishing returns function, r(m). ESS total ejaculate expenditure (the product m(*)s(*)) increases in all three models with sperm competition risk, q. If r(m), or ratio r'(m)/r(m), is independent of ESS sperm numbers, ESS sperm mass remains constant, and the sperm mass/number ratio (m(*)/s(*)) therefore decreases with risk. Dependency of sperm mass on risk can arise if r(m) depends on competing sperm density (sperm number / space available for sperm competition). Such dependencies generate complex relationships between sperm mass and number with risk, depending both on the mechanism and how sperm density affects r(m). While numbers always increase with risk, mass can either increase or decrease, but m(*)/s(*) typically decreases with risk unless sperm density strongly influences r(m). Where there is no extrinsic loading due to mating order, ESS paternity of the second (i.e. last) male to mate (P(2)) under displacement always exceeds 0.5, and increases with risk (in the raffle P(2)=0.5). Caution is needed when seeking evidence for a sperm size-number trade off. Although size and number trade-off independently against effort spent on acquiring matings, their product, m(*)s(*), is invariant or fixed at a given risk level, effectively generating a size-number trade off. However, unless controlled for the effects of risk, the relation between m(*) and s(*) can be either positive or negative (a positive relation is usually taken as evidence against a size-number trade off).


Subject(s)
Algorithms , Cell Size , Models, Biological , Spermatozoa/cytology , Animals , Female , Male , Reproduction , Risk Factors , Sexual Behavior, Animal , Sperm Count
3.
J Evol Biol ; 20(1): 381-91, 2007 Jan.
Article in English | MEDLINE | ID: mdl-17210031

ABSTRACT

Length of the sperm flagellum and of the female's primary sperm-storage organ, the seminal receptacle (SR), exhibit a pattern of rapid correlated evolution in Drosophila and other lineages. Experimental evolution studies with Drosophila melanogaster indicate that these traits have coevolved through sexual selection, with length of the SR representing the proximal basis of female sire discrimination, biasing paternity according to sperm length. Here, we examine the impact of experimentally varying the developmental environment, including larval density and larval and adult nutrition, on sperm length, SR length and on the pattern of sperm precedence. Expression of SR length was far more sensitive to variation among developmental environments than was sperm length. Nevertheless, there was striking co-variation in sperm and SR length. The developmental environment of both females and second males, but not first males, significantly contributed to variation in male competitive fertilization success.


Subject(s)
Biological Evolution , Drosophila melanogaster/physiology , Environment , Genitalia, Female/anatomy & histology , Selection, Genetic , Spermatozoa/cytology , Spermatozoa/physiology , Analysis of Variance , Animal Nutritional Physiological Phenomena/physiology , Animals , Female , Larva/physiology , Male , Sex Factors
4.
J Evol Biol ; 16(1): 114-26, 2003 Jan.
Article in English | MEDLINE | ID: mdl-14635886

ABSTRACT

Despite its central role in post-copulatory sexual selection, the female reproductive tract is poorly understood. Here we provide the first experimental study of the adaptive significance of variation in female sperm-storage organ morphology. Using populations of Drosophila melanogaster artificially selected for longer or shorter seminal receptacles, we identify relationships between the length of this primary sperm-storage organ and the number of sperm stored, pattern of progeny production, rate of egg fertilization, remating interval, and pattern of sperm precedence. Costs and benefits of relatively short or long organs were identified. Benefits of longer receptacles include increased sperm-storage capacity and thus progeny production from a single insemination. Results suggest that longer receptacles have not naturally evolved because of developmental time costs and a correlated reduction in longevity of mated females. This latter cost may be a consequence of sexual conflict mediated by ejaculate toxicity. Receptacle length did not alter the pattern of sperm precedence, which is consistent with data on the co-evolution of sperm and female receptacle length, and a pattern of differential male fertilization success being principally determined by the interaction between these male and female traits.


Subject(s)
Biological Evolution , Drosophila melanogaster/anatomy & histology , Drosophila melanogaster/physiology , Genitalia, Female/anatomy & histology , Selection, Genetic , Sex Characteristics , Animals , Body Weights and Measures , Female , Male , Reproduction/physiology , Spermatozoa/physiology
5.
Heredity (Edinb) ; 87(Pt 1): 25-32, 2001 Jul.
Article in English | MEDLINE | ID: mdl-11678984

ABSTRACT

The length of the female's primary sperm-storage organ, the seminal receptacle, has undergone rapid divergence within the Drosophila genus. Quantitative genetic analysis of seminal receptacle length was carried out on two laboratory strains of Drosophila melanogaster that had undergone artificial selection for both increased and decreased organ length. Realized heritabilities were 0.176 and 0.270 for the two experiments. Parental strains, F1, F1r (reciprocal), F2, backcross, and backcross reciprocal generations were used in a line-cross (generation means) analysis. This analysis revealed that additive, dominance, and additive-by-dominance epistasis contributed significantly to the means. No significant maternal effects were found. Variance analysis indicated that a completely additive model was adequate to explain the variances observed in these lines. Castle-Wright minimal estimates of 5.25 and 1.91, segregating loci responsible for mean differences, were found for the two respective experiments. There were significant positive correlations between additive effects of seminal receptacle length and thorax length in both experiments. The correlated evolution of sperm and seminal receptacle length is discussed.


Subject(s)
Drosophila melanogaster/anatomy & histology , Drosophila melanogaster/genetics , Animals , Biological Evolution , Female , Genetic Variation , Genitalia, Female/anatomy & histology , Heterozygote , Likelihood Functions , Male , Models, Genetic , Ovum/cytology , Quantitative Trait, Heritable , Selection, Genetic , Spermatozoa/cytology
6.
Proc Biol Sci ; 268(1471): 1071-80, 2001 May 22.
Article in English | MEDLINE | ID: mdl-11375092

ABSTRACT

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.


Subject(s)
Biological Evolution , Drosophila melanogaster/physiology , Pair Bond , Adaptation, Biological , Animals , Body Constitution , Female , Male , Spermatozoa/physiology
7.
Proc Biol Sci ; 268(1467): 557-63, 2001 Mar 22.
Article in English | MEDLINE | ID: mdl-11297171

ABSTRACT

The relatively small number of ova produced by a female can be fertilized by a single ejaculate in most species. Why females of many species mate with multiple males is therefore enigmatic, especially given that costs associated with remating have been well documented. Recently, it has been argued that females may remate at a maladaptive rate as an outcome of sexually antagonistic coevolution: the evolutionary tug-of-war between manipulation by one sex and resistance to being manipulated by the other sex. We tested this hypothesis experimentally for the evolution of the female remating interval in a naturally promiscuous species, Drosophila melanogaster. In two replicate populations, sexual selection was removed through enforced monogamous mating with random mate assignment, or retained in polyandrous controls. Monogamy constrains the reproductive success of mates to be identical, thereby converting prior conflicts between mates into opportunities for mutualism. Under these experimental conditions, the sexually antagonistic coevolution hypothesis generates explicit predictions regarding the direction of evolutionary change in female remating behaviour. These predictions are contingent upon the mechanism of male manipulation, which may be mediated biochemically by seminal fluids or behaviourally by courtship. Levels of divergence in female remating interval across lines, and in male ejaculatory and courtship effects on female remating, were quantified after 84 generations of selection. Data refute the hypothesis that the evolutionary change in female remating behaviour was due to sexually antagonistic coevolution of courtship signal and receiver traits. The data were, however, consistent with a hypothesis of sexual conflict mediated through ejaculate manipulation. Monogamy-line males evolved ejaculates that were less effective in inducing female non-receptivity and monogamy-line females evolved to remate less frequently, symptomatic of lowered resistance to ejaculate manipulation. The consistency of the results with alternative hypotheses to explain female promiscuity are discussed.


Subject(s)
Drosophila melanogaster/physiology , Sexual Behavior, Animal , Animals , Female , Male , Reproduction , Selection, Genetic
8.
Evolution ; 54(3): 1052-6, 2000 Jun.
Article in English | MEDLINE | ID: mdl-10937280
9.
Heredity (Edinb) ; 84 ( Pt 4): 416-26, 2000 Apr.
Article in English | MEDLINE | ID: mdl-10849065

ABSTRACT

Flies in the genus Drosophila have undergone striking evolutionary divergence in the size and number of sperm produced. Based on comparative studies of sperm length, testis length, and other reproductive and life history traits, including body size, age at first reproduction, and the number of sperm produced, macroevolutionary trade-offs resulting from the need to produce high-investment testes have been postulated. To understand better the microevolutionary processes underlying these interspecific patterns, we imposed replicated bidirectional selection for testis length for 11-12 generations on D. hydei, a species with 23.5 mm-long sperm and 30 mm-long testes. Testis length exhibited realized heritabilities ranging from 0.45 to 0.72. Following selection, traits were assayed for correlated responses. Thorax length, testis mass, sperm length, egg-to-adult development time, and posteclosion maturation time showed consistent positive correlated responses. Numbers of sperm produced and transferred to females, male longevity, female egg productivity, and seminal receptacle length did not show consistent correlated responses to selection on testis length. The pattern of correlated responses to testis length reveal the potential for the evolution of reproductive strategies to alter important life history attributes.


Subject(s)
Drosophila/growth & development , Drosophila/genetics , Life Cycle Stages , Animals , Body Constitution , Drosophila/anatomy & histology , Drosophila/physiology , Female , Male , Reproduction/physiology , Selection, Genetic , Testis/anatomy & histology , Testis/growth & development , Testis/physiology
10.
Curr Biol ; 9(20): R787-90, 1999 Oct 21.
Article in English | MEDLINE | ID: mdl-10531020

ABSTRACT

Genetic and cell biological analyses of sperm behavior in the female reproductive tract are providing important clues to the mechanisms of sperm competition, a form of sexual selection that is an important force that shapes reproductive behavior, physiology and morphology in a wide range of species.


Subject(s)
Fertilization/physiology , Spermatozoa/physiology , Animals , Caenorhabditis elegans/genetics , Caenorhabditis elegans/physiology , Disorders of Sex Development , Drosophila melanogaster/genetics , Drosophila melanogaster/physiology , Female , Fertilization/genetics , Male , Reproduction/genetics , Reproduction/physiology , Selection, Genetic
11.
Proc Biol Sci ; 265(1398): 821-6, 1998 May 07.
Article in English | MEDLINE | ID: mdl-9628039

ABSTRACT

Tails of fertilizing spermatozoa persist throughout embryogenesis in Drosophila species and can be observed within the midguts of larvae after hatching. Throughout development, sperm proteins slowly diffuse or are stripped from the giant sperm tail residing within the embryo's anterior end. The shape and position of the sperm within the embryo are regulated such that, during organ formation, the unused portion of the sperm is enveloped by the developing midgut. This persistent, paternally derived structure is composed of the sperm's mitochondrial derivatives and appears to be defecated by the larva soon after hatching. These complex sperm-egg interactions may represent mechanisms to avoid intragenomic conflict by ensuring strictly maternal inheritance of mitochondrial DNA (mtDNA).


Subject(s)
Drosophila/embryology , Drosophila/physiology , Sperm-Ovum Interactions/physiology , Animals , DNA, Mitochondrial/genetics , Female , Male
12.
J Mol Evol ; 43(3): 281-6, 1996 Sep.
Article in English | MEDLINE | ID: mdl-8703094

ABSTRACT

The phylogeny of the Drosophila hydei subgroup, which is a member of the D. repleta species group, was inferred from 1,515 base pairs of mitochondrial DNA sequence of the cytochrome oxidase subunits I, II, and III. Four of the seven species in the subgroup were examined, which are placed into two taxonomic complexes: the D. bifurca complex (D. bifurca and D. nigrohydei) and the D. hydei complex (D. hydei and D. eohydei). Both complexes appear to be monophyletic, although the D. bifurca complex is only weakly supported. The evolution of chromosomal change, interspecific crossability, sperm gigantism, and divergence times of the subgroup is discussed in a phylogenetic context.


Subject(s)
DNA, Mitochondrial/chemistry , Drosophila/classification , Drosophila/genetics , Electron Transport Complex IV/genetics , Phylogeny , Animals , Base Composition , Base Sequence , DNA, Mitochondrial/genetics , Drosophila/enzymology , Drosophila melanogaster/chemistry , Drosophila melanogaster/enzymology , Drosophila melanogaster/genetics , Electron Transport Complex IV/chemistry , Female , Karyotyping , Macromolecular Substances , Male , X Chromosome , Y Chromosome
14.
Trends Ecol Evol ; 11(4): 148-51, 1996 Apr.
Article in English | MEDLINE | ID: mdl-21237788
15.
Proc Natl Acad Sci U S A ; 92(23): 10614-8, 1995 Nov 07.
Article in English | MEDLINE | ID: mdl-7479851

ABSTRACT

Among fruit-fly species of the genus Drosophila there is remarkable variation in sperm length, with some species producing gigantic sperm (e.g., > 10 times total male body length). These flies are also unusual in that males of some species exhibit a prolonged adult nonreproductive phase. We document sperm length, body size, and sex-specific ages of reproductive maturity for 42 species of Drosophila and, after controlling for phylogeny, test hypotheses to explain the variation in rates of sexual maturation. Results suggest that delayed male maturity is a cost of producing long sperm. A possible physiological mechanism to explain the observed relationship is discussed.


Subject(s)
Drosophila/growth & development , Sexual Maturation/physiology , Spermatozoa/cytology , Animals , Body Constitution , Cell Size , Female , Male , Models, Biological , Phylogeny , Sex Characteristics , Species Specificity , Time Factors
17.
Proc Natl Acad Sci U S A ; 91(20): 9277-81, 1994 Sep 27.
Article in English | MEDLINE | ID: mdl-7937755

ABSTRACT

Males of the fruit fly Drosophila hydei were found to produce 23.47 +/- 0.46-mm-long spermatozoa, the longest ever described. No relationship was found between male body size and sperm length. We predicted that if these giant gametes are costly for males to produce, then correlations should exist between male body size, rates of sperm production, and fitness attributes associated with the production of sperm. Smaller males were found to make a greater relative investment in testicular tissue growth, even though they have shorter and thinner testes. Smaller males were also found to (i) be maturing fewer sperm bundles within the testes at any point in time than larger males, (ii) require a longer period of time post-eclosion to become reproductively mature, (iii) mate with fewer females, (iv) transfer fewer sperm per copulation, and (v) produce fewer progeny. The significance of these findings for body size-related fitness and the question of sperm size evolution are discussed.


Subject(s)
Biological Evolution , Drosophila/physiology , Spermatogenesis , Spermatozoa/physiology , Animals , Body Constitution , Body Weight , Drosophila/anatomy & histology , Female , Fertility , Male
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