scholarly journals Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes

2016 ◽  
Author(s):  
Anne Vielle ◽  
Nicolas Callemeyn-Torre ◽  
Clotilde Gimond ◽  
Nausicaa Poullet ◽  
Jeremy C. Gray ◽  
...  

AbstractSperm cells provide crucial, if usually diminutive, ingredients to successful sexual reproduction as the source of centrioles and half the diploid genome. Despite this essential conserved function, sperm competition and coevolution with female traits can drive spectacular change in size and shape of these motile cells. Here we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Exploring potential genetic and developmental determinants of Caenorhabditis sperm size variation, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes of androdioecious species, as well as within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development, i.e. at the formation of primary spermatocytes while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter-and intraspecific sperm size differences in Caenorhabditis. Together, our results provide a novel integrative view on the developmental and evolutionary origins of Caenorhabditis sperm size variation. We hypothesize that life history and/or ecological differences among species favoured the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm, with gigantic sperm potentially providing a means of paternal care via gametic provisioning or as a potent vehicle for sexual conflict over offspring development.

Evolution ◽  
2016 ◽  
Vol 70 (11) ◽  
pp. 2485-2503 ◽  
Author(s):  
Anne Vielle ◽  
Nicolas Callemeyn-Torre ◽  
Clotilde Gimond ◽  
Nausicaa Poullet ◽  
Jeremy C. Gray ◽  
...  

2005 ◽  
Vol 19 (1) ◽  
pp. 45-54 ◽  
Author(s):  
G. Bernasconi ◽  
B. Hellriegel
Keyword(s):  

2018 ◽  
Vol 30 (11) ◽  
pp. 1434 ◽  
Author(s):  
Tessa Pahl ◽  
Hanna J. McLennan ◽  
Yun Wang ◽  
Anang S. Achmadi ◽  
Kevin C. Rowe ◽  
...  

It is widely accepted that in mammals a causal relationship exists between postcopulatory sexual selection and relative testes mass of the species concerned, but how much it determines sperm size and shape is debatable. Here we detailed for the largest murine rodent tribe, the Rattini, the interspecific differences in relative testes mass and sperm form. We found that residual testes mass correlates with sperm head apical hook length as well as its angle, together with tail length, and that within several lineages a few species have evolved highly divergent sperm morphology with a reduced or absent apical hook and shorter tail. Although most species have a relative testes mass of 1–4%, these derived sperm traits invariably co-occur in species with much smaller relative testes mass. We therefore suggest that high levels of intermale sperm competition maintain a sperm head with a long apical hook and long tail, whereas low levels of intermale sperm competition generally result in divergent sperm heads with a short or non-existent apical hook and shorter tail. We thus conclude that sexual selection is a major selective force in driving sperm head form and tail length in this large tribe of murine rodents.


Evolution ◽  
2003 ◽  
Vol 57 (5) ◽  
pp. 1078-1088 ◽  
Author(s):  
Francisco García-González ◽  
Yolanda NÜÑEZ ◽  
Fernando Ponz ◽  
Eduardo R. S. Roldán ◽  
Montserrat Gomendio

2010 ◽  
Vol 6 (4) ◽  
pp. 513-516 ◽  
Author(s):  
Renée C. Firman ◽  
Leigh W. Simmons

Evolutionary biologists have argued that there should be a positive relationship between sperm size and sperm velocity, and that these traits influence a male's sperm competitiveness. However, comparative analyses investigating the evolutionary associations between sperm competition risk and sperm morphology have reported inconsistent patterns of association, and in vitro sperm competition experiments have further confused the issue; in some species, males with longer sperm achieve more competitive fertilization, while in other species males with shorter sperm have greater sperm competitiveness. Few investigations have attempted to address this problem. Here, we investigated the relationship between sperm morphology and sperm velocity in house mice ( Mus domesticus ). We conducted in vitro sperm velocity assays on males from established selection lines, and found that sperm midpiece size was the only phenotypic predictor of sperm swimming velocity.


2011 ◽  
Vol 278 (1721) ◽  
pp. 3135-3141 ◽  
Author(s):  
Montserrat Gomendio ◽  
Maximiliano Tourmente ◽  
Eduardo R. S. Roldan

The hypothesis that sperm competition should favour increases in sperm size, because it results in faster swimming speeds, has received support from studies on many taxa, but remains contentious for mammals. We suggest that this may be because mammalian lineages respond differently to sexual selection, owing to major differences in body size, which are associated with differences in mass-specific metabolic rate. Recent evidence suggests that cellular metabolic rate also scales with body size, so that small mammals have cells that process energy and resources from the environment at a faster rate. We develop the ‘metabolic rate constraint hypothesis’ which proposes that low mass-specific metabolic rate among large mammals may limit their ability to respond to sexual selection by increasing sperm size, while this constraint does not exist among small mammals. Here we show that among rodents, which have high mass-specific metabolic rates, sperm size increases under sperm competition, reaching the longest sperm sizes found in eutherian mammals. By contrast, mammalian lineages with large body sizes have small sperm, and while metabolic rate (corrected for body size) influences sperm size, sperm competition levels do not. When all eutherian mammals are analysed jointly, our results suggest that as mass-specific metabolic rate increases, so does maximum sperm size. In addition, species with low mass-specific metabolic rates produce uniformly small sperm, while species with high mass-specific metabolic rates produce a wide range of sperm sizes. These findings support the hypothesis that mass-specific metabolic rates determine the budget available for sperm production: at high levels, sperm size increases in response to sexual selection, while low levels constrain the ability to respond to sexual selection by increasing sperm size. Thus, adaptive and costly traits, such as sperm size, may only evolve under sexual selection when metabolic rate does not constrain cellular budgets.


2008 ◽  
Vol 20 (4) ◽  
pp. 474 ◽  
Author(s):  
B. B. Dzyuba ◽  
K. J. W. Van Look ◽  
V. S. Kholodnyy ◽  
N. Satake ◽  
S. Cheung ◽  
...  

Like seahorses, some of the closely-related pipefish species (Family Syngnathidae) incubate their eggs within a male brood pouch. This has contributed to considerable confusion about sperm transfer mechanisms to the eggs; some authors have reported that ejaculates are released directly into water before they reach the eggs, while others have suggested that eggs are fertilised using spermatozoa deposited directly into the brood pouch via an internal sperm duct. Here we present anatomical evidence from the freshwater pipefish, Syngnathus abaster, showing not only that direct sperm deposition into the pouch is impossible, but that spermatozoa must somehow travel a significant distance (>4 mm) outside the body of the male, to reach and fertilise eggs in the pouch. We have also used several putative sperm-activating solutions to identify the type of environment most conducive to sperm activation. Spermatozoa released from the testis were active for a brief period (<5 min) in water or 150 mm saline, but showed prolonged (>25 min) motility in ovarian fluid. This suggests that spermatozoa are released into a mixture of ovarian fluid and eggs while the male and female are in close contact. Our data also suggest that the fertilisation mechanism is highly efficient (sperm : egg ratio <200 : 1) even though this pipefish species produces dimorphic spermatozoa (with long and short flagellae). The shorter (<40 μm) morphotypes were not capable of motility activation, and are therefore probably incapable of fertilisation. If so, the sperm : egg ratio reported here would represent an overestimate.


Sign in / Sign up

Export Citation Format

Share Document