Abstract
Sexual selection favors the evolution of pre-copulatory sexual traits such as ornamentation and post-copulatory sexual traits such as long sperm, but the interrelationships of the two types of sexual traits remain unclear. Here, using Japanese barn swallows, Hirundo rustica gutturalis, and an interspecific analysis of the family Hirundinidae, we examined sperm length in relation to pheomelanin-based plumage coloration. As predicted by the fact that pheomelanogenesis consumes antioxidants, which would be detrimental to develop long sperm, reddish coloration (but not other ornaments) were negatively related to sperm length both within and across species, suggesting an evolutionary tradeoff between these traits.
Avoid common mistakes on your manuscript.
Sexual selection favors the evolution of pre-copulatory sexual traits that enhance mating success via mate choice and intrasexual contest (e.g., conspicuous ornaments; reviewed in Andersson 1994). Likewise, sexual selection favors the evolution of post-copulatory sexual traits, enhancing fertilization success via sperm choice/competition (e.g., long sperm; Bennison et al. 2015; reviewed in Birkhead and Møller 1998). The two evolutionary processes might not be independent if pre- and post-copulatory sexual traits are interrelated: positive relationship facilitates and negative relationship constrains the evolution of sexual traits. Therefore, it is important to know whether and how the two types of sexual traits are interrelated.
Concerning this point, two alternative hypotheses are proposed with particular attention to oxidative stress due to our understanding that sperm quality is susceptible to oxidative stress (reviewed in Friesen et al. 2020). First, the redox-based “phenotype-linked fertility hypothesis” predicts a positive relationship between pre- and post-copulatory sexual traits based on the assumption that individuals with enough supply of resources (antioxidants) invest more in both pre- and post-copulatory sexual traits (Sheldon 1994; Blount et al. 2001). Second, “sperm competition theory” predicts a negative relationship between them, because resources (e.g., antioxidants) invested in pre-copulatory sexual traits is unavailable for post-copulatory sexual traits, or vice versa (Parker 1998; Tazzyman et al. 2009). Although empirical studies of animals, particularly those with carotenoid-based coloration (i.e., a sexual trait that uses dietary antioxidants), sometimes found positive (e.g., Helfenstein et al. 2010) and negative relationships (e.g., Rowe et al. 2010), no clear pattern was observed across studies (reviewed in Mautz et al. 2013).
Pheomelanin is a reddish-brown pigment widespread among birds and mammals (McGraw 2006). In contrast to carotenoids, (pheo)melanin pigments are synthesized in animals, and are long thought to be mostly independent of individual physiological state or resource availability (e.g., McGraw 2008; Roulin 2016). However, pheomelanogenesis consumes glutathione, an important antioxidant, and thus phaeomelanin production trades off with anti-oxidative defence (e.g., Ito and Wakamatsu 2008; Galván and Alonso-Alvarez 2009; Arai et al. 2017). Therefore, as is the case for carotenoid-based coloration, pheomelanin-based coloration would affect sperm quality, because glutathione is potentially linked to sperm quality as an antioxidant (Friesen et al. 2020), and because consumption of an antioxidant (glutathione) affects other antioxidants as well (Blount et al. 2001).
The barn swallow, Hirundo rustica, is a model species for pre- and post-copulatory sexual selection (Møller 1994; Turner 2006). They have several sexually selected ornaments, including pheomelanin-based reddish throat coloration (reviewed in Romano et al. 2017). Extrapair paternity is generally high (e.g., ca. 20% of young in the European subspecies, H. r. rustica) but varies markedly across populations, and sperm morphology tracks the frequency of extrapair paternity in each population (i.e., small and variable sperm in a population with low extrapair paternity; Laskemoen et al. 2013; Hasegawa et al. 2019). Although sperm quality is found to be related to some traits in this species (e.g., Møller et al. 2008 for covariation between sperm swimming performance and male tarsus length), the relationship between pheomelanin-based coloration and sperm quality has not been reported.
Here, we examined sperm length in relation to pheomelanic plumage coloration in Joetsu population of the Asian barn swallow (H. r. gutturalis). They have reddish throat patches that are twice as large as those of European ones (Hasegawa et al. 2010a). In this low-density population (ca. 20 m between the nearest breeding males), extrapair paternity is virtually absent (< 3% of young: Hasegawa et al. 2010b), and hence small and variable sperm length is observed (Hasegawa et al. 2019). This population provides a unique opportunity to examine how intense pre-copulatory, but not post-copulatory, sexual selection affects sperm quality and its relationship with pre-copulatory sexual traits (see Hasegawa 2018 for a review of sexual selection in Japanese populations). We predicted a negative relationship between sperm length and throat coloration, because spermiogenesis, including the sperm elongation process, is easily affected by oxidative stress (e.g., see Ricketts et al. 2011 for in vivo and in vitro experiments in Drosophila: note that this is also important in vertebrate; Henkel 2011), and because pheomelanin-based reddish throat coloration is shown to be negatively related to oxidative balance in Japanese barn swallows even during the breeding period (e.g., Arai et al. 2017, 2018). We also tested the interspecific patterns using the family Hirundinidae.
Methods
Study site
The current study was conducted during the early breeding season (1 April–30 June) in 2017 and 2018 in a residential area of the Joetsu City, Niigata Prefecture, Japan (37°07′N, 138°15′E). We inspected nests every third day to record breeding events.
Capture and measurement
Adults were captured in sweep nets while roosting at night. Each bird was provided with a numbered aluminum ring and a unique combination of half-sized colored rings. The sex of each individual was determined by the tail shape and by the presence (female) or absence (male) of an incubation patch (Turner 2006). We obtained ejaculate samples by gently massaging the males’ cloacal protuberance and measured sperm sizes afterwards (Hasegawa et al. 2019). Detailed measurements are given in Supplementary material 1.
We measured wing length, tarsus length, keel length, body mass, and four measures of plumage ornaments, i.e., outermost tail feather length, the size of white-tail spots, throat patch size, and throat coloration at capture (see Hasegawa et al. 2010a for details). Detailed information on measuring coloration is given in Supplementary material 2.
Statistics
We standardized all measurements to zero mean and unit variance in each study year to exclude possible year effects before analysis (see Table S1). Body condition index was calculated as residual body mass on keel length after standardizing each variable in each year (linear model: coefficient ± SE = 0.52 ± 0.21, F1,17 = 6.44, P = 0.02). We also conducted phylogenetic comparative analysis using the family Hirundinidae (see Supplementary material 3 for details). All data analyses (e.g., Pearson’s product-moment correlation, multiple linear model) were performed using the R statistical package (ver. 4.0.0; R Core Team 2020).
Results
Sperm length was not significantly correlated with male ornaments (Pearson’s product-moment correlation coefficient, |r|< 0.38, n = 19, P > 0.10) except for throat coloration value: Males with redder throats had shorter sperm (r = 0.50, n = 19, P = 0.029; Fig. 1). Each component of sperm, i.e., sperm head length, midpiece length, and tail length was not significantly correlated with male ornaments (i.e., outermost tail feather length, the size of white-tail spots, throat patch size, and throat coloration: |r|< 0.45, n = 19, P > 0.05). Qualitatively similar results were found when we used multiple linear models to exclude the possible confounding effects of other ornaments, although the sample size was limited (Table 1).
Wing length, tarsus length, keel length, body mass, and body condition were not significantly correlated with sperm length (|r|< 0.31, P > 0.19), and its components (|r|< 0.44, P > 0.06). Neither body mass nor body condition index was significantly related to male ornaments in the current data set (|r|< 0.29, n = 19, P = 0.22).
When using a phylogenetic comparative analysis while controlling for the extrapair mating opportunity (see Supplementary material 3), we found that species with reddish plumage had significantly shorter sperm than species without reddish plumage (Fig. 2; Table 2).
Discussion
We found a negative relationship between sperm length and pheomelanic reddish plumage coloration both within and across species, as predicted by sperm competition theory (see Introduction). Confounding effects of other ornamental traits and its correlates (e.g., age) are unlikely, because we found no detectable correlations between sperm sizes and other ornaments including a highly age-dependent trait (i.e., outermost tail feather length; e.g., Hasegawa et al. 2010a). To our knowledge, the current study is the first study demonstrating a negative relationship between sperm size and pheomelanin-based coloration in any animal species and clades.
A simple explanation for the observed pattern is that pre-copulatory sexual selection favors the evolution of pheomelanin-rich throat patches at the expense of sperm size by consuming glutathione, an antioxidant. Because extrapair paternity is virtually absent in the study population, post-copulatory sexual selection for long sperm would be negligible (see Introduction), possibly contributing to uncovering the tradeoff (due to the limited confounding effects of extrapair mating; also see Table 2 for the interspecific pattern controlling for the extrapair mating opportunity). In addition to such a direct tradeoff, selection for more pheomelanin (i.e., selection for glutathione consumption for pigmentation) might indirectly favor short sperm, because long sperm is more likely to be affected by oxidative stress (e.g., Hermosell et al. 2013). Another explanation that less-colorful males invest more in sperm competition (i.e., have longer sperm) is unlikely due to the lack of extrapair paternity (see above; note that the rare paternity loss was found in males with small white-tail spots rather than males with the colorful throat; Hasegawa 2018).
The current correlational study, however, could not exclude all confounding factors. Because colorful males hold high-quality territories in this population (Hasegawa et al. 2014), intense agonistic interaction for such preferable territories might increase energy expenditure and reduce male physiological conditions as well (though colorful males often have better body conditions than drab males: e.g., Arai et al. 2018). Likewise, via intraspecific interactions, pheomelanic coloration feeds back their physiological state (including oxidative balance) in barn swallows (e.g., Safran et al. 2008; Vitousek et al. 2013), and thus behavioral interaction would reinforce the relationship between oxidative balance and plumage coloration (Arai et al. 2018). These phenotypic plasticities alone cannot explain the observed interspecific pattern, which suggests an evolutionary tradeoff between the two kinds of sexual traits, constraining the evolution of each sexual trait. The causality behind the relationship, however, remains to be clarified, possibly with experimental manipulation of oxidative status.
Data availability
The datasets were uploaded to osf.io (https://doi.org/10.17605/osf.io/b5cs7).
Change history
10 December 2022
A Correction to this paper has been published: https://doi.org/10.1007/s10164-022-00775-w
References
Andersson M (1994) Sexual selection. Princeton Univ Press, Princeton
Arai E, Hasegawa M, Makino T, Hagino A, Sakai Y, Ohtsuki H, Wakamatsu K, Kawata M (2017) Physiological conditions and genetic controls of phaeomelanin pigmentation in nestling barn swallows. Behav Ecol 28:706–716
Arai E, Hasegawa M, Ito S, Wakamatsu K (2018) Males with more pheomelanin have a lower oxidative balance in Asian barn swallows (Hirundo rustica gutturalis). Zool Sci 35:505–513
Bennison C, Hemmings N, Slate J, Birkhead T (2015) Long sperm fertilize more eggs in a bird. Proc R Soc Lond B 282:20141897
Birkhead T, Møller AP (1998) Sperm competition and sexual selection. Academic Press, London
Blount JD, Møller AP, Houston DC (2001) Antioxidants, showy males and sperm quality. Ecol Lett 4:393–396
Friesen CR, Noble DWA, Olsson M (2020) The role of oxidative stress in postcopulatory selection. Phil Trans R Soc B 375:20200065
Galván I, Alonso-Alvarez C (2009) The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proc R Soc B 276:3089–3097
Hasegawa M (2018) Sexual selection mechanisms for male plumage ornaments in Japanese Barn Swallows. Ornithol Sci 17:125–134
Hasegawa M, Arai E, Watanabe M, Nakamura M (2010a) Mating advantage of multiple male ornaments in the Barn Swallow Hirundo rustica gutturalis. Ornithol Sci 9:141–148
Hasegawa M, Arai E, Kojima W, Kitamura W, Fujita G, Higuchi H, Watanabe M, Nakamura M (2010b) Low level of extra-pair paternity in a population of the Barn Swallow Hirundo rustica gutturalis. Ornithol Sci 9:161–164
Hasegawa M, Arai E, Watanabe M, Nakamura M (2014) Colourful males hold high quality territories but exhibit reduced paternal care in barn swallows. Behaviour 151:591–612
Hasegawa M, Arai E, Nakamura M (2019) Small and variable sperm in a barn swallow population with low extra pair paternity. Zool Sci 36:154–158
Helfenstein F, Losdat S, Møller AP, Blount JD, Richner H (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222
Henkel RR (2011) Leukocytes and oxidative stress: dilemma for sperm function and male fertility. Asian J Androl 13:43–52
Hermosell IG, Laskemoen T, Rowe M, Møller AP, Mousseau TA, Albrecht T, Lifjeld JT (2013) Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity. Biol Lett 9:20130530
Ito S, Wakamatsu K (2008) Chemistry of mixed melanogenesis–Pivotal roles of dopaquinone. Photochem Photobiol 84:582–592
Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, de Lope F, Hermosell IG et al (2013) Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol 67:301–309
Mautz BS, Møller AP, Jennions MD (2013) Do male secondary sexual characters signal ejaculate quality? A meta-analysis. Biol Rev 88:669–682
McGraw KJ (2006) Mechanics of melanin-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1. mechanisms and measurements. Harvard Univ Press, Cambridge, pp 243–294
McGraw KJ (2008) An update on the honesty of melanin-based color signals in birds. Pigm Cell Melanoma Res 21:133–138
Møller AP (1994) Sexual selection and the barn swallow. Oxford Univ Press, Oxford
Møller AP, Mousseau TA, Rudolfsen G (2008) Females affect sperm swimming performance: a field experiment with barn swallows Hirundo rustica. Behav Ecol 19:1343–1350
Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, San Diego, pp 3–49
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Ricketts P-GA, Minimair M, Yates RW, Klaus A (2011) The effects of glutathione, insulin and oxidative stress on cultured spermatogenic cysts. Spermatogenesis 1:159–171
Romano A, Constanzo A, Rubolini D, Saino N, Møller AP (2017) Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta-analysis. Biol Rev 92:1582–1600
Roulin A (2016) Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin-based colouration. Biol Rev 91:328–348
Rowe M, Swaddle JP, Pruett-Jones S, Webster MS (2010) Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairywren. Anim Behav 79:1239–1246
Safran RJ, Adelman JS, McGraw KJ, Hau M (2008) Sexual signal exaggeration affects physiological state in male barn swallows. Curr Biol 18:R461–R462
Sheldon BC (1994) Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257:25–30
Tazzyman SJ, Pizzari T, Seymour RM, Pomiankowski A (2009) The evolution of continuous variation in ejaculate expenditure strategy. Amer Natl 174:E71–E82
Turner AK (2006) The barn swallow. T and AD Poyser, London
Vitousek MN, Stewart RA, Safran RJ (2013) Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird. Biol Lett 9:20130539
Acknowledgements
We are grateful to the residents of Joetsu City for their kind support and assistance. We also thank Dr. Shumpei Kitamura and his laboratory members in Ishikawa Prefectural University. MH was supported by the Research Fellowship of the Japan Society for the Promotion of Science (JSPS, 19K06850).
Author information
Authors and Affiliations
Contributions
MH did most field survey, performed statistical analysis, and wrote most of the manuscript, EA and MN assisted field survey, provided technical support and improved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
We have no conflict of interest.
Ethical approval
The permits for animal capture and handling were provided by Niigata Prefecture in Japan (#1 and #24 for 2017 and 2018, respectively), following the Wildlife Protection and Hunting Management Law.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised due to a retrospective Open Access order
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Hasegawa, M., Arai, E. & Nakamura, M. Reddish male swallows have short sperm. J Ethol 40, 85–89 (2022). https://doi.org/10.1007/s10164-021-00726-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-021-00726-x