No Evidence for Pre-Copulatory Sexual Selection on Sperm Length in a Passerine Bird

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection

Species-level divergences in multiple functional traits between the two endemic subspecies of Blue Chaffinches Fringilla teydea in Canary Islands

Background: One of the biggest challenges in avian taxonomy is the delimitation of allopatric species because their reproductive incompatibility cannot be directly studied in the wild. Instead, reproductive incompatibility has to be inferred from multiple, divergent character sets that indicate a low likelihood of allopatric populations amalgamating upon secondary contact. A set of quantitative criteria for species delimitation has been developed for avian taxonomy. Results: Here, we report a broad multi-trait comparison of the two insular subspecies of the Blue Chaffinch Fringilla teydea, endemic to the pine forests of Tenerife (ssp. teydea) and Gran Canaria (ssp. polatzeki) in the Canary Islands. We found that the two taxa were reciprocally monophyletic in their whole mitogenomes and two Z chromosome introns. The genetic distance in mitogenomes indicates around 1 Mya of allopatric evolution. There were diagnostic differences in body morphometrics, song and plumage reflectance spectra, whose combined divergence score (=11) exceeds the threshold level (=7) set for species delimitation by Tobias et al. (Ibis 152:724–746, 2010). Moreover, we found a marked divergence in sperm lengths with little range overlap. Relatively long sperm with low intra- and intermale CV compared to other passerines suggest a mating system with high levels of sperm competition (extrapair paternity) in these taxa. Conclusion: The large and diagnostic divergences in multiple functional traits qualify for species rank, i.e., Tenerife Blue Chaffinch (Fringilla teydea) and Gran Canaria Blue Chaffinch (Fringilla polatzeki). We encourage a wider use of sperm traits in avian taxonomy because sperm divergences might signal reproductive incompatibility at the postcopulatory prezygotic stage, especially in species with sperm competition

Sperm Length Variation as a Predictor of Extrapair Paternity in Passerine Birds

The rate of extrapair paternity is a commonly used index for the risk of sperm competition in birds, but paternity data exist for only a few percent of the approximately 10400 extant species. As paternity analyses require extensive field sampling and costly lab work, species coverage in this field will probably not improve much in the foreseeable future. Recent findings from passerine birds, which constitute the largest avian order (∼5,900 species), suggest that sperm phenotypes carry a signature of sperm competition. Here we examine how well standardized measures of sperm length variation can predict the rate of extrapair paternity in passerine birds.We collected sperm samples from 55 passerine species in Canada and Europe for which extrapair paternity rates were already available from either the same (n = 24) or a different (n = 31) study population. We measured the total length of individual spermatozoa and found that both the coefficient of between-male variation (CV(bm)) and within-male variation (CV(wm)) in sperm length were strong predictors of the rate of extrapair paternity, explaining as much as 65% and 58%, respectively, of the variation in extrapair paternity among species. However, only the CV(bm) predictor was independent of phylogeny, which implies that it can readily be converted into a currency of extrapair paternity without the need for phylogenetic correction.We propose the CV(bm) index as an alternative measure to extrapair paternity for passerine birds. Given the ease of sperm extraction from male birds in breeding condition, and a modest number of sampled males required for a robust estimate, this new index holds a great potential for mapping the risk of sperm competition across a wide range of passerine birds

Age before beauty? Relationships between fertilization success and age-dependent ornaments in barn swallows

When males become more ornamented and reproduce more successfully as they grow older, phenotypic correlations between ornament exaggeration and reproductive success can be confounded with age effects in cross-sectional studies, and thus say relatively little about sexual selection on these traits. This is exemplified here in a correlative study of male fertilization success in a large colony of American barn swallows (Hirundo rustica erythrogaster). Previous studies of this species have indicated that two sexually dimorphic traits, tail length and ventral plumage coloration, are positively correlated with male fertilization success, and a mechanism of sexual selection by female choice has been invoked. However, these studies did not control for potential age-related variation in trait expression. Here, we show that male fertilization success was positively correlated with male tail length but not with plumage coloration. We also show that 1-year-old males had shorter tails and lower fertilization success than older males. This age effect accounted for much of the covariance between tail length and fertilization success. Still, there was a positive relationship between tail length and fertilization success among older males. But as this group consisted of males from different age classes, an age effect may be hidden in this relationship as well. Our data also revealed a longitudinal increase in both tail length and fertilization success for individual males. We argue that age-dependent ornament expression and reproductive performance in males complicate inferences about female preferences and sexual selection

Male age is associated with extra-pair paternity, but not with extra-pair mating behaviour

Extra-pair paternity is the result of copulation between a female and a male other than her social partner. In socially monogamous birds, old males are most likely to sire extra-pair offspring. The male manipulation and female choice hypotheses predict that age-specific male mating behaviour could explain this old-over-young male advantage. These hypotheses have been difficult to test because copulations and the individuals involved are hard to observe. Here, we studied the mating behaviour and pairing contexts of captive house sparrows, Passer domesticus. Our set-up mimicked the complex social environment experienced by wild house sparrows. We found that middle-aged males, which would be considered old in natural populations, gained most extra-pair paternity. However, both, female solicitation behaviour and subsequent extra-pair matings were not associated with male age. Further, copulations were more likely when solicited by females than when initiated by males (i.e. unsolicited copulations). Male initiated within-pair copulations were more common than male initiated extra-pair copulations. To conclude, our results did not support either hypothesis regarding age-specific male mating behaviour. Instead, female choice, independent of male age, governed copulation success, especially in an extra-pair context. Post-copulatory mechanisms might determine why older males sire more extra-pair offspring

Intraspecific variation in sperm length in two passerine species, the Bluethroat Luscinia svecica and the Willow Warbler Phylloscopus trochilus

Sperm cells are highly diversified in birds and considerable research effort has focused on variation in sperm morphology between species. However, surprisingly little is known about intraspecific variation in sperm morphology in birds. We analyzed between-and within-male variation in total sperm length in two passerine species, the Bluethroat (Luscinia svecica) and the Willow Warbler (Phylloscopus trochilus). In both species, the variance in sperm length was nearly twice as high between as within males, resulting in high repeatability of sperm length for individual males (Bluethroat: r = 0.73 and Willow Warbler: r = 0.79). These results suggest that sperm traits are more variable among than within males. With a resampling approach, we illustrate how the spread in estimated mean sperm length and coefficient of variation (CV) is affected by increasing the number of males measured. Further, we illustrate how the CV of sperm length for individual males change with the number of spermatozoa measured. For the two species in our analyses, it seems that measuring 10 males and 10 spermatozoa per male gives adequate estimates of both between-and within-male sperm length and CV

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology

This is the peer-reviewed version of the following article: Rowe, M., Albrecht, T., Cramer, E. R., Johnsen, A., Laskemoen, T., Weir, J. T., & Lifjeld, J. T. (2015). Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology. Evolution, 69(4), 1044-1052, which has been published in final form at https://doi.org/10.1111/evo.12620. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.Rapid diversification of sexual traits is frequently attributed to sexual selection, though explicit tests of this hypothesis remain limited. Spermatozoa exhibit remarkable variability in size and shape, and studies report a correlation between sperm morphology (sperm length and shape) and sperm competition risk or female reproductive tract morphology. However, whether postcopulatory processes (e.g., sperm competition and cryptic female choice) influence the speed of evolutionary diversification in sperm form is unknown. Using passerine birds, we quantified evolutionary rates of sperm length divergence among lineages (i.e., species pairs) and determined whether these rates varied with the level of sperm competition (estimated as relative testes mass). We found that relative testes mass was significantly and positively associated with more rapid phenotypic divergence in sperm midpiece and flagellum lengths, as well as total sperm length. In contrast, there was no association between relative testes mass and rates of evolutionary divergence in sperm head size, and models suggested that head length is evolutionarily constrained. Our results are the first to show an association between the strength of sperm competition and the speed of sperm evolution, and suggest that postcopulatory sexual selection promotes rapid evolutionary diversification of sperm morphology.This work was supported by the Research Council of Norway grant 196554 (to JTL). In addition, JTW acknowledges a Discovery Grant from the National Sciences and Engineering Research Council of Canada, TA acknowledges a grant from the Czech Science Foundation (project P506/12/2472), and MR acknowledges a Young Research Talent grant from the Research Council of Norway (230434/F20)