Pavlína Opatová

Inbreeding depression of sperm traits in the zebra finch Taeniopygia guttata.

Abstract Inbreeding depression, or the reduction in fitness due to mating between close relatives, is a key issue in biology today. Inbreeding negatively affects many fitness‐related traits, including survival and reproductive success. Despite this, very few studies have quantified the effects of inbreeding on vertebrate gamete traits under controlled breeding conditions using a full‐sib mating approach. Here, we provide comprehensive evidence for the negative effect of inbreeding on sperm traits in a bird, the zebra finch Taeniopygia guttata. We compared sperm characteristics of both inbred (pedigree F = 0.25) and outbred (pedigree F = 0) individuals from two captive populations, one domesticated and one recently wild‐derived, raised under standardized conditions. As normal spermatozoa morphology did not differ consistently between inbred and outbred individuals, our study confirms the hypothesis that sperm morphology is not particularly susceptible to inbreeding depression. Inbreeding did, however, lead to significantly lower sperm motility and a substantially higher percentage of abnormal spermatozoa in ejaculate. These results were consistent across both study populations, confirming the generality and reliability of our findings.

A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success

Male reproductive success depends on the competitive ability of sperm to fertilize the ova, which should lead to strong selection on sperm characteristics. This raises the question of how heritable variation in sperm traits is maintained. Here we show that in zebra finches (Taeniopygia guttata) nearly half of the variance in sperm morphology is explained by an inversion on the Z chromosome with a 40% allele frequency in the wild. The sperm of males that are heterozygous for the inversion had the longest midpieces and the highest velocity. Furthermore, such males achieved the highest fertility and the highest siring success, both within-pair and extra-pair. Males homozygous for the derived allele show detrimental sperm characteristics and the lowest siring success. Our results suggest heterozygote advantage as the mechanism that maintains the inversion polymorphism and hence variance in sperm design and in fitness.It is unclear how variation in sperm traits is maintained in nature. Here, the authors show that an inversion on the Z chromosome of zebra finches affects sperm morphology and fertilization ability and suggest that overdominance maintains the inversion polymorphism.

Trade-off between carotenoid-based sexual ornamentation and sperm resistance to oxidative challenge

It has been hypothesized that carotenoid-based sexual ornamentation signals male fertility and sperm competitive ability as both ornamentation and sperm traits may be co-affected by oxidative stress, resulting in positive covariation (the ‘redox-based phenotype-linked fertility hypothesis’; redox-based PLFH). On the other hand, the ‘sperm competition theory’ (SCT) predicts a trade-off between precopulatory and postcopulatory traits. Here, we manipulate oxidative status (using diquat dibromide) and carotenoid availability in adult zebra finch (Taeniopygia guttata) males in order to test whether carotenoid-based beak ornamentation signals, or is traded off against, sperm resistance to oxidative challenge. Initial beak colouration, but not its change during the experiment, was associated with effect of oxidative challenge on sperm velocity, such that more intense colouration predicted an increase in sperm velocity under control conditions but a decline under oxidative challenge. This suggests a long-term trade-off between ornament expression and sperm resistance to oxidative challenge. Shortening of the sperm midpiece following oxidative challenge further suggests that redox homeostasis may constrain sperm morphometry. Carotenoid supplementation resulted in fewer sperm abnormalities but had no effect on other sperm traits. Overall, our data challenge the redox-based PLFH, partially support the SCT and highlight the importance of carotenoids for normal sperm morphology.

Testing the phenotype-linked fertility hypothesis in the presence and absence of inbreeding

The phenotype‐linked fertility hypothesis suggests that females can judge male fertility by inspecting male phenotypic traits. This is because male sexually selected traits might correlate with sperm quality if both are sensitive to factors that influence male condition. A recent meta‐analysis found little support for this hypothesis, suggesting little or no shared condition dependence. However, we recently reported that in captive zebra finches (Taeniopygia guttata) inbreeding had detrimental effects both on phenotypic traits and on measures of sperm quality, implying that variation in inbreeding could induce positive covariance between indicator traits and sperm quality. Therefore, we here assess empirically the average strength of correlations between phenotypic traits (courtship rate, beak colour, tarsus length) and measures of sperm quality (proportion of functional sperm, sperm velocity, sperm length) in populations of only outbred individuals and in mixed populations consisting of inbreds (F = 0.25) and outbreds (F = 0). As expected, phenotype sperm‐trait correlations were stronger when the population contained a mix of inbred and outbred individuals. We also found unexpected heterogeneity between our two study populations, with correlations being considerably stronger in a domesticated population than in a recently wild‐derived population. Correlations ranged from essentially zero among outbred‐only wild‐derived birds (mean Fishers Zr ± SE = 0.03 ± 0.10) to moderately strong among domesticated birds of mixed inbreeding status (Zr ± SE = 0.38 ± 0.08). Our results suggest that, under some conditions, the phenotype‐linked fertility hypothesis might apply.

Do ornaments, arrival date, and sperm size influence mating and paternity success in the collared flycatcher?

Males advertise their intrinsic parental and/or genetic qualities by the size of secondary sexual ornaments. Moreover, they compete with one another for the best territory and males who arrive first at the breeding ground usually have an advantage in this competition. Females may consider multiple male qualities simultaneously and prefer the one most important for their fitness in the current context. They can further improve their fitness by selecting the best care-giver as their social mate and engaging in an extra-pair copulation with a genetically superior male. In such cases, sperm competition arises in the female reproductive tract and its outcome may be affected by the sperm morphology of both the social and extra-pair male. Here, we tested these ideas in the collared flycatcher (Ficedula albicollis), a species with context-dependent choice of social partners and frequent extra-pair paternity. We recorded male arrival to breeding sites, manipulated their forehead patches, and measured sperm size. In contrast to a previous study in a Swedish population, males with enlarged patches were non-significantly less successful late in the season while no such difference was found early in the season. Besides this tendential seasonal interaction, arrival date did not affect mating and paternity success or male fitness, and the same was true for sperm size. These results suggest different benefits of male ornamentation and female mate choice between populations and call for more replicated research within and between species.Significance statementThe fitness of a male of a migratory species might be affected by several pathways. First, early arrival should confer benefits in the form of best territory choice. Second, in a dichromatic and sexually promiscuous species, secondary sexual ornaments are considered by females both in the choice of social and extra-pair mates. Third, by modifying sperm traits, males may outmatch their rivals in sperm competition. These ideas have usually been tested in isolation. In this experimental study, we tested the joint effect of all of these factors on the genetic fitness of males. We found little evidence for the dependence of male reproductive success on either sperm morphology or plumage ornamentation which is in contrast to other populations of the species. Our study calls for replicated research both in well-established fields like mate choice and emerging ones like sperm competition.