The evolutionary implications of polyandry in house mice (Mus domesticus) /

[Truncated abstract] Despite the costs associated with mating, females of many taxa solicit multiple mates during a single reproductive event (polyandry). Polyandry is clearly adaptive when females gain direct benefits from males at mating. However, polyandry has also been shown to increase female fitness in the absence of direct benefits. Thus, a number of genetic benefit hypotheses have been developed to account for the origin of this behaviour. Although not mutually exclusive, a distinction lays between genetic benefits that propose defense against reproductive failure (nonadditive genetic effects), and those that propose benefits from intrinsic sire effects (additive genetic effects). Nonadditive genetic benefits of polyandry have been documented in a number of species; by soliciting multiple mates females can avoid inbreeding and other forms of incompatibility between parental genotypes. Polyandry may also increase female reproductive success when genetically superior males have greater success in sperm competition, and produce better quality offspring. An inevitable consequence of polyandry is that sperm from rival males will overlap in the female reproductive tract and compete to fertilise the ova. The outcome of sperm competition is typically determined by bias in sperm use by the females, interactions between parental genotypes, and ejaculate characteristics that provide a fertilisation advantage. Thus, sperm competition is recognised as a persuasive force in the evolution of male reproductive traits. Comparative analyses across species, and competitive mating trials within species have suggested that sperm competition can influence the evolution of testis size and sperm production, and both sperm form and sperm function. ... After six generations of selection I observed phenotypic divergence in litter size - litter size increased in the polyandrous lines but not in the monandrous lines. This result was not attributable to inbreeding depression, or environmental/maternal effects associated with mating regime. Genetic benefits associated with polyandry could account for this result if increased litter size were attributable to increased embryo survival. However, males from the polyandrous lineages were subject to sperm competition, and evolved ejaculates with more sperm, suggesting that evolutionary increases in litter size may in part be due to improved male fertility. Finally, Chapter Five is an investigation of the natural variation in levels of polyandry in the wild, and the potential for sperm competition to drive macroevolutionary changes in male reproductive traits among geographically isolated island populations of house mice. I sampled seven island populations of house mice along the coast of Western Australia and, by genotyping pregnant females and their offspring, determined the frequency of multiply sired litters within each population. I applied the frequency of multiple paternity as an index of the risk of sperm competition, and looked for selective responses in testis size and ejaculate traits. I found that the risk of sperm competition predicted testis size across the seven island populations. However, variation in sperm traits was not explained by the risk of sperm competition. I discuss these results in relation to sperm competition theory, and extrinsic factors that influence ejaculate quality.Thesis (Ph.D.)--University of Western Australia, 2008[Truncated abstract] Despite the costs associated with mating, females of many taxa solicit multiple mates during a single reproductive event (polyandry). Polyandry is clearly adaptive when females gain direct benefits from males at mating. However, polyandry has also been shown to increase female fitness in the absence of direct benefits. Thus, a number of genetic benefit hypotheses have been developed to account for the origin of this behaviour. Although not mutually exclusive, a distinction lays between genetic benefits that propose defense against reproductive failure (nonadditive genetic effects), and those that propose benefits from intrinsic sire effects (additive genetic effects). Nonadditive genetic benefits of polyandry have been documented in a number of species; by soliciting multiple mates females can avoid inbreeding and other forms of incompatibility between parental genotypes. Polyandry may also increase female reproductive success when genetically superior males have greater success in sperm competition, and produce better quality offspring. An inevitable consequence of polyandry is that sperm from rival males will overlap in the female reproductive tract and compete to fertilise the ova. The outcome of sperm competition is typically determined by bias in sperm use by the females, interactions between parental genotypes, and ejaculate characteristics that provide a fertilisation advantage. Thus, sperm competition is recognised as a persuasive force in the evolution of male reproductive traits. Comparative analyses across species, and competitive mating trials within species have suggested that sperm competition can influence the evolution of testis size and sperm production, and both sperm form and sperm function. ... After six generations of selection I observed phenotypic divergence in litter size - litter size increased in the polyandrous lines but not in the monandrous lines. This result was not attributable to inbreeding depression, or environmental/maternal effects associated with mating regime. Genetic benefits associated with polyandry could account for this result if increased litter size were attributable to increased embryo survival. However, males from the polyandrous lineages were subject to sperm competition, and evolved ejaculates with more sperm, suggesting that evolutionary increases in litter size may in part be due to improved male fertility. Finally, Chapter Five is an investigation of the natural variation in levels of polyandry in the wild, and the potential for sperm competition to drive macroevolutionary changes in male reproductive traits among geographically isolated island populations of house mice. I sampled seven island populations of house mice along the coast of Western Australia and, by genotyping pregnant females and their offspring, determined the frequency of multiply sired litters within each population. I applied the frequency of multiple paternity as an index of the risk of sperm competition, and looked for selective responses in testis size and ejaculate traits. I found that the risk of sperm competition predicted testis size across the seven island populations. However, variation in sperm traits was not explained by the risk of sperm competition. I discuss these results in relation to sperm competition theory, and extrinsic factors that influence ejaculate quality

SLIRP KO males produce smaller litters and have fewer progressively motile sperm.

<p>(A) Litter sizes resulting from breeding wild type (WT) females with WT or SLIRP knockout (KO) males (*, significant difference by Maximum Likelihood analysis of repeated measures, p = 0.025). (B) Comparison of daily sperm production (B), motility (C) and progressive motility (D) between WT and SLIRP KO animals. **, ANOVA, p&lt;0.001.</p

SLIRP is expressed in the mouse testis.

<p>(A &amp; B) Detection of SLIRP by immunohistochemistry in Leydig cells, spermatogonia (green arrow), early spermatocytes (yellow arrows), round spermatids (red arrows), elongate spermatids and sperm lining the lumen (white arrows). (C, F, I) Immunofluorescent staining for SLIRP (green), (D) Hsp60 (red), PCNA (G, red) and SP56 (J, red) overlayed in E, H &amp; K respectively. Yellow indicates colocalization in overlayed panels. Nuclear DAPI staining in blue E, H &amp; K. White bars: A, 80 µm, B, H &amp; K, 10 µm, E, 20 µm.</p

SLIRP localization in epididymal sperm.

<p>(A) Immunofluorescent staining for SLIRP (green) and Sp56 (B, red) in sperm heads (C, overlay). (D) SLIRP (green) and Septin 4 (E, red) staining of sperm tails (F, overlay). White bars: C, 10 µm; F, 1 µm.</p

Generation of the SLIRP KO mouse.

<p>(A) Wild type (WT), floxed SLIRP and SLIRP knockout (KO) mouse SLIRP locus configurations. Floxed mice contain a cDNA for SLIRP exons 2 to 4 (Ex 2–4) with polyadenylation signal (poly A) preceded by loxp and splice acceptor (SA) sites and followed by loxp, SA, Flag epitope, stop codon and c-<i>fos</i> sequences inserted within the first SLIRP intron (intron length in kb, nt, nucleotides). (B) Southern analysis to detect a 31.3 kb EcoRV fragment in WT (+/+) and heterozygous (+/−) mice and a 13.3 kb recombinant band in heterozygous and SLIRP homozygous KO (−/−) animals. (C) WT (334 nt) and recombinant (247 nt) RT-PCR products generated from WT and recombinant SLIRP mouse liver cDNAs. (D) Western analysis of WT and recombinant SLIRP mouse testis lysates for SLIRP and β–actin.</p

Annulus and mitochondrial disruption in SLIRP KO sperm.

<p>Electron micrographs of the distal mid-piece and annulus region of (A) WT and (B) SLIRP KO sperm. White arrows, annulus; white bar, abnormal mid-piece/annulus junction in KO sperm; black arrows, electron light and dense areas in WT and KO mitochondria respectively. Black bars, 0.5 µm.</p