Rapid evolution of sperm length in response to increased temperature in an ectothermic fish

The Intergovernmental Panel on Climate Change predicts an average global temperature increase of 1.8–4.0 °C by 2100. Tropical ectotherms are expected to be particularly sensitive to this temperature increase because they live close to their thermal limits. We investigated the phenotypic plasticity and evolutionary response of sperm traits in guppies (Poecilia reticulata) to increased temperatures after 6, 18, and 24 months. Guppies with evolution temperatures of 25 °C (control) or 28 °C were reared in either 25 or 28 °C in a 2 × 2 common garden design. The plastic response to increased temperature was a decreased sperm length, velocity, and path linearity. The evolutionary response was a subsequent increase in sperm length, resulting in complete compensation after just 6 months (at most four generations) in 28 °C water. Sperm velocity and linearity showed no sign of evolution even after 24 months. This study provides evidence that some reproductive traits can respond via rapid evolution to the temperature increase associated with climate change.     

The evolution of sperm morphometry in pheasants

Post-copulatory sexual selection is thought to be a potent evolutionary force driving the diversification of sperm shape and function across species. In birds, insemination and fertilization are separated in time and sperm storage increases the duration of sperm-female interaction and hence the opportunity for sperm competition and cryptic female choice. We performed a comparative study of 24 pheasant species (Phasianidae, Galliformes) to establish the relative importance of sperm competition and the duration of sperm storage for the evolution of sperm morphometry (i.e. size of different sperm traits). We found that sperm size traits were negatively associated with the duration of sperm storage but were independent of the risk of sperm competition estimated from relative testis mass. Our study emphasizes the importance of female reproductive biology for the evolution of sperm morphometry particularly in sperm-storing taxa.     

The molecular evolution of sperm zonadhesin

Based on pioneering work of Hardy and Garbers, zonadhesin has become one of the best studied sperm ligands in boreoeutherian mammals, both from a biochemical and evolutionary perspective. Zonadhesin is a mosaic-type protein that localizes to the apical head of spermatozoa. In pig, cattle, rabbit and primates, zonadhesin precursor essentially consists of two or three MAM (meprin/A5 antigen/mu receptor tyrosine phosphatase) domains, one mucin-like domain, one incomplete and four complete D domains (homologous to vWFD). Mouse zonadhesin is distinguished from this general pattern by 20 extra partial D3 domains. While concerted evolution drives the divergence of the mucin-like domain in the ortholog comparison, MAM and D domains mainly diverge under the influence of drift and positive selection, both in the paralog and ortholog comparison. As can be seen particularly well within a putative binding region in the most C-terminal MAM domain, positive selection not only causes amino acid exchanges, but also promotes changes in the pattern of predicted posttranslational modification. Moving window and correlation analyses of sequence evolution and sexual body dimorphism further suggest that sexual selection, especially sperm competition, drives zonadhesin divergence. However, considering its zona pellucida avidity, female cryptic choice might as well contribute to zonadhesin evolution. Despite the general tendency for divergence of zonadhesin, conservation by negative selection dominates the evolution of most codon sites. In accordance, the distribution of EGF (epidermal growth factor)-like motifs, DP-doublets, single cysteines and CGLC motifs suggests a wide conservation of processing, folding and oligomerization of zonadhesin in pig, rabbit and primates.     

A polypeptide sperm activator from male Saturniid moths

When the mature sperm of Saturniid moths are ejaculated during copulation, they are mixed in the male's common duct with a secretion which induces vigorous motility in the sperm. The active substance in this secretion is soluble in 7·5% trichloroacetic acid but not in organic solvents; it is stable in aqueous solution at 100°C, but is only partially dialysable. These properties plus the fact that activity is completely destroyed by proteolytic enzymes suggest that the substance is a polypeptide. When filtered through Sephadex columns, all of the activity can be resolved into a single peak corresponding to a molecular weight between 1600 and 4500, most probably about 3100. Even in highly active preparations this peak could not be detected with ninhydrin reagent. Calculations indicate that the lowest concentration of activator that will induce motility is not more than 10⁻⁸m. Most naturally occurring substances having properties similar to those of the activator have proved to be hormones.     

The evolution of sea urchin sperm bindin

Sea urchins have been model organisms for the study of fertilization for more than a century. Fertilization in sea urchins happens externally, which facilitates the study of sperm-egg attachment and fusion, and means that all of the molecules involved in gamete recognition and fusion are associated with the gametes. Sea urchin sperm bindin was the first "gamete recognition protein" to be isolated and characterized (Vacquier and Moy 1977), and bindin has since been studied by developmental biologists interested in fertilization, by biochemists interested in membrane fusion and by evolutionary biologists interested in reproductive isolation and speciation. Research on bindin was last reviewed thirteen years ago by Vacquier et al. (1995) in an article titled "What have we learned about sea urchin sperm bindin?" in which the authors reviewed the identification, isolation and early molecular examinations of bindin. Research since then has focused on bindin's potential role in fusing egg and sperm membranes, comparisons of bindin between distantly related species, studies within genera linking bindin evolution to reproductive isolation, and studies within species looking at fertilization effects of individual bindin alleles. In addition, the egg receptor for bindin has been cloned and sequenced. I review this recent research here.     

The length scale of selection in protein evolution

Central to the study of molecular evolution, and an area of long-standing debate, is the appropriate model for the fitness landscape of proteins. Much of this debate has focused on the strength and frequency of positive and purifying selection, but the form and frequency of selective correlations is also a vital element. The constituent amino acids within a protein generically interact and share selective pressures in predictable ways, which conflicts with the selective independence assumed by common caricatures of the fitness landscape. Here, I discuss a recent study by myself and coauthors that used whole-genome comparisons of orthologous molecular sequences from closely related Drosophilids to explore the form of the selective correlations and selective interactions (epistasis) between the amino acids within a protein. I outline our results and highlight our finding of a selective length scale of ten amino acids within which individual amino acids are substantially and generically more likely to share selective pressures and interact epistatically. I then focus on the evidence presented in our study supporting a substantial role for epistasis in the process of molecular evolution, and discuss further the implications of this widespread epistasis on the overdispersion of the molecular clock and the efficacy of common tests for positive selection.     

The evolution of sperm transfer mechanisms in the Diptera

The known occurrence of spermatophores in the Diptera and some possible modes of transition to other mechanisms of sperm transfer are outlined. The closed systems of transfer, and the significance of modifications of gonopore shape in some species, are discussed.     

The Y chromosome and sperm length in D. melanogaster

Contrary to earlier reports, the sperm length of D. melanogaster males with two Y chromosomes is the same as in males with one Y chromosome.     

Intron length evolution in Drosophila

I present data on the evolution of intron lengths among 3 closely related Drosophila species, D. melanogaster, Drosophila simulans, and Drosophila yakuba. Using D. yakuba as an outgroup, I mapped insertion and deletion mutations in 148 introns (spanning approximately 30 kb) to the D. melanogaster and D. simulans lineages. Intron length evolution in the 2 sister species has been different: in D. melanogaster, X-linked introns have increased slightly in size, whereas autosomal ones have decreased slightly in size; in D. simulans, both X-linked and autosomal introns have decreased in size. To understand the possible evolutionary causes of these lineage- and chromosome-specific patterns of intron evolution, I studied insertion-deletion (indel) polymorphism and divergence in D. melanogaster. Small insertion mutations segregate at elevated frequencies and enjoy elevated probabilities of fixation, particularly on the X chromosome. In contrast, there is no detectable X chromosome effect on fixations in D. simulans. These findings suggest X chromosome-specific selection or biased gene conversion-gap repair favoring insertions in D. melanogaster but not in D. simulans. These chromosome- and lineage-specific patterns of indel substitution are not easily explained by existing general population genetic models of intron length evolution. Genomic data from D. melanogaster further suggest that the forces described here affect introns and intergenic regions similarly.     

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.     

Testis asymmetry and sperm length in Rhacophorus omeimontis

Theory predicts that the degree of testes asymmetry should be positively correlated with male body condition in species with directional testis asymmetry. We tested this prediction in Rhacophorus omeimontis, a species in which females mate with more than one male. Our results showed that the treefrogs did not exhibit the absence of directional asymmetry in testis size, but rather the occurrence of fluctuating asymmetry. Moreover, we also tested differences in body size, body mass, testis mass, testis asymmetry, and sperm size among initially paired, jointly paired, and unpaired males. We found that body size and mass, testis mass, testis asymmetry and sperm length did not differ among the three male types. Testis mass showed a positive relationship with soma mass, but the correlations between the extent of fluctuating testis asymmetry and sperm length, and between testis mass and sperm length were not significant. Our data suggest that testes size and sperm length do not play an important role in determining male mating success in the presence of sperm competition.     

The role of wing length in the evolution of avian flightlessness

Flightlessness has evolved independently in at least 11 extant avian families. A number of hypotheses have been proposed to explain these transitions in individual families, including release from predation on oceanic islands, energetic costs of flight and use of forelimbs for activities other than flying. Few studies have sought to explore factors common to all families containing flightless species, which may explain the taxonomic distribution of flightlessness. In this study, we found that for all eight avian families which contain both flightless and flighted species, the flighted species have shorter wing lengths relative to body mass than their sister families. This result is not biased by taxon size. Models of avian aerodynamics predict that birds with relatively short wings pay a high energetic cost of flight. We suggest that these increased energetic costs of flying predispose these avian families to evolve flightless species. The various causes for the shortening of wings among flighted species of birds and the possibility of future transitions to flightlessness are discussed.     

Chemical constraints on the evolution of olfactory communication channels of moths

It is estimated there are over 100,000 moth species (Lepidoptera) that produce sex pheromones comprising communication channels used in specific-mate-recognition systems (SMRS) involved in pre-zygotic mating isolation and speciation. About 1572 moth species have been found to use 377 pheromone components, the majority being alcohols, aldehydes or acetate esters of olefinic chains of 10-22 carbons. Since there are limited numbers of possible unsaturated (double bonded) E- and Z-configured isomers of these chains, there may be constraints on incipient species evolving new pheromone components, especially if they are utilized by existing species. Here I develop algorithms that count and name all possible structures of chains with or without a functional group. The results show that for acetate esters there are only seven or nine monounsaturated isomers of six or seven carbon chains, respectively, suggesting use of these compounds could limit the number of communication channels available for radiation of new species (no moths use these short chains). For commonly used 14-carbon chains with an acetate ester functional group, and 1-3 unsaturations, there are 1039 isomers. A total of 2,096,883 isomers were counted from all multiply unsaturated 10-22-carbon chain acetate esters. The number of possible signals quickly extends into millions when considering pheromone blends of 2-4 components used by most species. There should be little chemical constraint on evolution of new communication channels based on compounds of 10 or more carbons, even for closely related species (e.g. ermine moths, Yponomeuta).     

Intra-individual variation in sperm tail length in murine rodents

In eutherian mammals, there are marked interspecific differences in sperm head shape and tail length. In a few species, sperm head variability occurs but intra-individual variation in sperm tail length has rarely been investigated or commented upon. Here, we ask the question: Do murine rodent species that have variable sperm head shapes exhibit greater intra-individual variation in sperm midpiece and total tail lengths than closely related species where little, or no, sperm head variability occurs? From three separate lineages, we selected three pairs of murine rodents, one of which has monomorphic, and the other variable, sperm head shape. These were from southern Asia the bandicoot rats Bandicota bengalensis and Bandicota indica , from southern Africa the veld rats, Aethomys chrysophilus and Aethomys ineptus and from Australia the fawn hopping mouse Notomys cervinus and the spinifex hopping mouse Notomys alexis . Cauda epididymal sperm smears were prepared and sperm midpiece and total tail lengths were determined. A linear mixed-effects model was used to estimate intra-individual variance. The results showed that in all three species where there are variable sperm head shapes ( B. indica , A. ineptus and N. alexis ), statistically significantly greater intra-individual variability of sperm midpiece and total tail lengths occurs ( P <0.0001 in all cases). These species all have relatively smaller testes mass compared with the closely related species with monomorphic sperm populations. This suggests that depressed levels of intermale sperm competition may result in the occurrence of variability in not only the divergent sperm head shape but also in the length of the midpiece as well as that of the total length of the sperm tail.     

The evolution of sperm ultrastructure among Boidae (Serpentes)

We investigate the evolution of sperm ultrastructure of three species of Boidae (Epicrates cenchria, Boa constrictor amarali, and Corallus hortulanus). Spermatozoa of these species are filiform consisting of a head region, containing the nucleus and acrosome complex, a midpiece, and a tail region subdivided into principal piece and endpiece. Multilaminar membranes and extracellular microtubules were observed next to the plasma membrane of the spermatozoa. The following differences were observed among the species: ridge on acrosome surface in Boa constrictor amarali (absent in Epicrates cenchria and Corallus hortulanus), stopper-like perforatorium base plate in Boa constrictor amarali and Epicrates cenchria (absent in Corallus hortulanus), rounded mitochondria in transverse section in Epicrates cenchria and Corallus hortulanus (irregular in Boa constrictor amarali). We mapped sperm characters onto two phylogenies based on morphological (Kluge in Misc Publ Mus Zool Univ Michigan 178:1–58, 1991) and molecular (Austin in Copeia 2:341–352, 2000) data, using a number of squamate species as outgroups. We identified 31 unambiguous character transformations in the morphological phylogeny and 30 in the molecular phylogeny, but only 13 and 12 transformations, respectively, are possible synapomorphies. We identified novel sperm synapomorphies, which were common between the morphological and molecular phylogenies: absence of perforatorium base plate and mitochondria arranged as sinuous tubes in oblique section (Serpentes), acrosome vesicle not subdivided and fibers 3 and 8 at the anteriormost region of principal piece (Boidae), and absence of an electron dense structure inside the proximal centriole (Elapidae + Colubridae). Our results suggest greater agreement between sperm ultrastructure and gross anatomical characters. In addition, we found no tendency for more homoplasies in the sperm head than in the flagellum, as recorded in previous studies.     

Experimental evolution of sperm competitiveness in a mammal

Background  

When females mate with multiple partners, sperm from rival males compete to fertilise the ova. Studies of experimental evolution have proven the selective action of sperm competition on male reproductive traits. However, while reproductive traits may evolve in response to sperm competition, this does not necessarily provide evidence that sperm competitive ability responds to selection. Indeed, a study of Drosophila failed to observe divergence in sperm competitive ability of males in lines selected for enhanced sperm offence and defence.     

Sperm length evolution in the fungus-growing ants

Eusocial insects offer special opportunities for the comparativestudy of sperm traits because sperm competition is absent (inspecies with obligatory monandry) or constrained (in lineageswhere queens mate multiply but never remate later in life).We measured sperm length in 19 species of fungus-growing ants,representing 9 of the 12 recognized genera, and mapped theseonto the ant phylogeny. We show that average sperm length acrossspecies is highly variable and decreases with mature colonysize in basal genera with singly mated queens, suggesting thatsperm production or storage constraints affect the evolutionof sperm length. Sperm length does not decrease further in multiplymating leaf-cutting ants, despite substantial further increasesin colony size. In a combined analysis, sexual dimorphism explained63.1% of the variance in sperm length between species. As colonysize was not a significant predictor in this analysis, we concludethat sperm production trade-offs in males have been the majorselective force affecting sperm length across the fungus-growingants, rather than storage constraints in females. The relationshipbetween sperm length and sexual dimorphism remained robust inphylogenetically independent contrasts. Some of the remainingvariation was explained by the relative size of the sperm-storageorgan, but only in the multiply mating leaf-cutting ants, suggestingthat sperm-storage constraints become important for the evolutionof sperm length in this derived group. Mate number affectedsperm length to a minor extent, and only in interaction withother predictor variables, suggesting that sperm competitionhas not been a major selective force for sperm length evolutionin these ants.