# Offspring's early-life performance varies with father's sperm quality in a genetically monogamous seabird

Frédéric Manas, Maxime Pineaux, Ségolène Humann-Guilleminot, Scott A

Hatch, Pierrick Blanchard, Sarah Leclaire

► To cite this version:

Frédéric Manas, Maxime Pineaux, Ségolène Humann-Guilleminot, Scott A Hatch, Pierrick Blanchard, et al.. Offspring's early-life performance varies with father's sperm quality in a genetically monogamous seabird. Behavioral Ecology and Sociobiology, 2024, 78 (11), pp.118. 10.1007/s00265-024-03540-w. hal-04802123

HAL Id: hal-04802123

https://hal.science/hal-04802123v1

Submitted on 26 Nov 2024

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# Offspring's early-life performance varies with father's sperm quality in a genetically monogamous seabird

Frédéric Manas¹ID · Maxime Pineaux¹ID · Ségolène Humann-Gilleminot²ID · Scott A. Hatch³ID

Pierrick Blanchard¹ID · Sarah Leclaire¹ID

Received: 3 September 2024 / Revised: 4 November 2024 / Accepted: 8 November 2024

© The Author(s) 2024

## Abstract

Although the effect of sperm quality is well studied in the context of sperm competition, its effect on offspring performance, especially after the embryo stages, has been less investigated. Here, we investigated whether the proportion of spermatozoa with normal morphology was associated with offspring performance during chick development in the black-legged Kittiwake, a behaviorally and genetically monogamous seabird in which sperm competition is absent. First, we found that, at hatching, the difference in body condition between the first- and second-hatched siblings was higher when the father had a lower proportion of normal spermatozoa. We discuss this result in light of maternal allocation strategy to manipulate sibling competition. Second, we showed that, in first-hatched chicks, body mass growth between hatching and the age of 10 days, body condition at the age of 10 days and maximum body mass reached before fledging were positively related to the proportion of normal spermatozoa in the father's sperm. Overall, our results support the role of sperm quality on offspring performance in the black-legged Kittiwake and call for further studies investigating the importance of sperm quality in genetically monogamous species.

## Significance statement

The importance of sperm quality has been poorly studied in other contexts than sperm competition. We show that, in a genetically monogamous seabird, the mass growth and condition of first-hatched chicks increase with the proportion of normal spermatozoa in the father's sperm. Unexpectedly, our results further suggest that females might differentially invest into eggs according to traits correlated with the quality of their partner's sperm.

**Keywords** Black-legged Kittiwake · Chick · Fitness · Sperm morphology · Monogamy · *Rissa tridactyla*

## Introduction

Fifty years ago, sperm competition (i.e., the competition between the ejaculates of different males for fertilization of a given set of ova) was suggested to contribute to sexual selection (Parker 1970) and to drive the evolution of numerous physiological, behavioral or morphological adaptations in males and females (Wigby and Chapman 2004; Pizzari and Parker 2009). Since then, a large number of studies have focused on sperm quality (e.g., spermatozoa number, morphology, motility) in promiscuous species (Pizzari and Parker 2009; Simmons and Fitzpatrick 2012; Fitzpatrick and Lüpold 2014; Lüpold et al. 2020; Macartney et al. 2024). They revealed that sperm quality, affecting the fertilization potential of a male (Firman and Simmons 2009), is under stronger selection when sperm competition is more intense

Pierrick Blanchard and Sarah Leclaire are co-last authors.

Communicated by C. R. Brown.

<figure><img src="image_2.png" /></figure>

Sarah Leclaire
sarah.leclaire@univ-tlse3.fr

<footnote n="1">¹ Centre de Recherche sur la Biodiversité et l'Environnement (CRBE), Université de Toulouse, CNRS, IRD, Toulouse INP, Université Toulouse 3 - Paul Sabatier (UT3), Toulouse, France</footnote>

<footnote n="2">² Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum d'Histoire Naturelle, CNRS, SU, EPHE, UA, Paris, France</footnote>

<footnote n="3">³ Institute for Seabird Research and Conservation, Anchorage, AK 99516, USA</footnote>
(Immler et al. 2008; Firman and Simmons 2009, 2011; van der Horst and Maree 2014; Lüpold and Pitnick 2018).

In contrast, much less attention has been given to sperm quality in genetically monogamous species, where sperm competition is absent. Van der Horst and Maree (2014) showed that in a few monogamous species, sperm show severe morphological abnormalities. They suggested that “in the absence of sperm competition, there may be little benefit in investing energy on the quality of sperm produced” (van der Horst and Maree 2014). However, sperm quality not only affects sperm competition outcome, but also offspring performance. For instance, low quality ejaculate can affect embryo development, via genetic or epigenetic alterations of sperm cell DNA or poor composition of the seminal fluid (Morgan and Watkins 2020; Watkins et al. 2020). Such effects can also extend beyond birth (Fernández-Gonzalez et al. 2008). Accordingly, cryopreservation reduces larval growth after hatching in brown trouts (*Salmo trutta*) (Nusbaumer et al. 2019), experimentally-prolonged sperm storage impairs son’s sperm quality in guppies (*Poecilia reticulata*) (Gasparini et al. 2017) and quality of seminal fluid affects offspring survival from hatching to adulthood in crickets (*Teleogryllus oceanicus*) (Simmons and Lovegrove 2019). Therefore, although sexual selection on sperm quality is relaxed in monogamous species (van der Horst and Maree 2014; Koffler et al. 2016), the effects of sperm quality on male reproductive success may still act as a natural selective pressure maintaining sperm quality in these species also.

Here, we investigated the potential for natural selection to act on the evolution of sperm quality in monogamous birds, by testing the association between sperm morphology and offspring performance in the black-legged Kittiwake (*Rissa tridactyla*). In this species, extra-pair copulations are very rare (<1% of all copulations) and extra-pair young are nearly inexistent (Helfenstein et al. 2004). The black-legged Kittiwake is thus considered as a behaviorally and genetically monogamous bird, in which sperm competition is absent (Helfenstein et al. 2004). As a proxy of sperm quality, we considered the proportion of spermatozoa with normal morphology, because in numerous species, abnormal sperm morphology is associated with altered metabolites in seminal plasma, and genetic or epigenetic modifications (Pukažhenthi et al. 2001; Boissonnas et al. 2010; Peng et al. 2019; Daneshmandpour et al. 2020; Mehrparvar et al. 2020). We tested whether sperm morphology affected offspring performance during chick development by focusing on chick body condition, body mass growth rate, and maximum body mass (i.e., peak mass) reached before fledging. We studied several nestling traits because those that determine fitness at adulthood (e.g., survival and lifetime reproductive success) are mostly unknown in Kittiwakes. However, chick growth

is probably an important component of fitness, because faster growing chicks are more likely to recruit in the colony (Coulson and Porter 1985; Vincenzi et al. 2015). In addition, in numerous birds, faster-growing or larger offspring have increased survival (Gebhardt-Henrich and Richner 1998; Ronget et al. 2018), and are assumed to recruit earlier, be better competitors for mates and access higher-quality breeding sites (Cam and Aubry 2011). If males with higher proportion of normal spermatozoa have better reproductive success, we predicted these males to sire chicks that grow faster and reach higher body mass. Finally, as male quality may correlate with both sperm morphology (Blount et al. 2001; Helfenstein et al. 2010) and male or female parental care (Burley 1988; Clutton-Brock 1991; Leclaire et al. 2011), we cross-fostered chicks just before hatching to limit the potential confounding effect of parental care to interfere with the relationship between sperm morphology and chick performance.

# Materials and methods

## Study site

The study was carried out in a natural population of black-legged Kittiwakes nesting on an abandoned US Air Force tower on Middleton Island, Gulf of Alaska, USA (59° 26' N, 146° 20' W). The nest sites created on the upper part of the tower can be observed from inside through sliding one-way windows and birds can be individually identified using color and metal bands (Gill and Hatch 2002). To investigate the association between sperm morphology and offspring performance at hatching, we used data collected in 2017 and 2018. In contrast, to investigate the associations between sperm morphology and offspring performance at post-hatching stages, we focused on data collected during a cross-fostering experiment carried out in 2018, in order to limit a confounding effect of parental care on the relationship between sperm quality and post-hatching chick performance. We collected sperm (see below) during the pre-laying period (2017: May 10 - June 6; 2018: May 17 – May 29). Because we were interested in the relationship between sperm quality and chick performance, we focused on sperm samples collected from males whose partner laid at least one egg. In this population, most birds lay two eggs, that hatch in the order of oviposition (hereafter, first- and second-laid eggs are named A- and B-eggs respectively), and one-egg and three-egg clutches are rare. Therefore, we focused our analyses on males who had a two-egg clutch. One male was captured both in 2017 and 2018.

In 2018, we conducted a cross-fostering experiment. Eggs were placed in an incubator three days before the expected
hatching date. Parents were given dummy eggs to incubate while their eggs were in the incubator. Chicks hatched in the incubator, and were put back in foster nests within 24 h after hatching. Siblings were not cross-fostered in the same nest. All chicks fostered as A-chicks came from A-eggs. We did not study cross-fostered B-chicks because most of them died before reaching the age of ten days (see below). Age difference between A- and B- foster siblings varied between 0 and 2 days which is the natural hatching asynchrony in this population of Kittiwakes (Gill et al. 2002). Because of other studies being carried out on the same birds, the cross-fostering experiment was not conducted randomly, but was based on the sex of the chicks. In this experiment, the proportion of normal spermatozoa was not related to the sex of the sired chicks (Student test: $t_{1,31} = 1.08, P=0.29$) or the sex of the adopted chicks (Student test: $t_{1,13} = 0.63, P=0.53$). We thus assumed that the cross-fostering experiment was carried out randomly according to the proportion of normal spermatozoa. Two broods that were not cross-fostered and one brood where siblings were cross-fostered together in the same nest were excluded from the analyses on post-hatching traits.

## Sperm collection and analysis

Sperm was collected using a non-invasive method described in Humann-Guilleminot et al. (2018). The head of the bird was placed in a cloth bag for ease of handling and to limit the stress associated with capture. A massage was then applied to the lower back and base of the tail. The sperm was collected with a 75 µL capillary placed on top of the cloaca, as close as possible to the tail. The sperm was immediately spread on a microscope slide, 5 µL of formalin was added and the slide was left for 30 min in the open air to dry. The slides were then analyzed in the laboratory using an Olympus BX-51 light microscope at a magnification of 100 times.

We classified the first 40 spermatozoa observed on a slide as normal or abnormal according to the parameters used in black-legged Kittiwakes (Humann-Guilleminot et al. 2018) and other species (De Vos et al. 2003; Auger 2010; Humann-Guilleminot et al. 2018). A spermatozoon considered as abnormal had certain types of deformations preventing its viability: a double or cut flagellum, an absent, curved, double or cut head, a deformation of the cytoplasm or the absence of an intermediate piece. This yielded to a total number of 31 sperm samples ($n=9$ males in 2017 and $n=22$ males in 2018, including 16 males whose A-chicks were included in the cross-fostering experiment). The proportion of normal spermatozoa was not significantly different between 2017 and 2018 (mean ± SE = $0.41 ± 0.05$ and $0.36 ± 0.04$, respectively; t test: $t_{1,29} = 0.76, P=0.45$). In addition, it varied neither with the date of sampling nor with the number of days between the date of sampling and the

date of laying (Pearson's correlation tests: $r=0.08, P=0.65$ and $r=0.02, P=0.90$, respectively), suggesting that the sperm sample collected is representative of that the female received during mating.

## Chick traits

Nests were checked twice daily, at 9:00 a.m. and 6:00 p.m., to record laying, hatching, death or disappearance of chicks throughout the study period. Eggs were labeled individually with a nontoxic marker on the day of laying, and chicks were marked on the head with similar markers for identification shortly after hatching. Most of the eggs hatched (54 eggs hatched, while 8 eggs did not hatch). Chicks were measured every 5 days from hatching to day 35 post-hatch. In black-legged Kittiwakes, although fledging occurs on ca. day 43 post-hatch (Coulson and Porter 1985), we did not manipulate chicks after day 35 post-hatch to avoid precocious fledging (Merkling et al. 2014). Body mass was measured to the nearest 0.1 g using an electronic scale and tarsus length to the nearest 0.1 mm with a caliper. Chick traits were measured blind to the father's sperm quality.

Because the effect of sperm quality on offspring may depend on the age of the chick (Evans et al. 2017), we analyzed the association between sperm morphology and offspring performance at different stages of chick development. We estimated the body condition of chicks at hatching and at day 10 post-hatch by calculating the residuals of a linear model explaining the body mass by the tarsus length (Merkling et al. 2014; Pineaux et al. 2020). This method is considered to give a good indicator of body condition in Kittiwakes (Jacobs et al. 2012). In Kittiwakes, most chicks reach a maximum body mass a few days before fledging, and then lose about 10% of body mass before fledging (Coulson and Porter 1985; Vincenzi et al. 2013). We therefore estimated the maximum body mass reached during the fledging period as the maximum mass recorded for a given chick, which usually occurs between day 30 and 35 post-hatch. We also estimated body mass growth rate over the first 10 days post-hatch and between day 10 and 25 post-hatch by calculating the slope of the linear regression between body mass and age. The analyses on body condition at hatching was carried out on chicks hatched in 2017 and 2018, while the analyses on post-hatching traits was carried out on cross-fostered chicks hatched in 2018. In addition, because most cross-fostered B-chicks (8 out of 14 chicks; 57%) died before the age of ten days, while no cross-fostered A-chicks died before the age of ten days, we restricted the analyses on chick post-hatching traits to cross-fostered A-chicks ($n=16$ chicks). Sample sizes for each fitness trait used in this study can be found in Table S1. Body condition at day 10 post-hatch was negatively correlated with body condition at hatching and
positively correlated with body mass growth rate between day 0 and day 10 post-hatch (Table S2), while all other correlation tests between fitness traits were not significant (Table S2).

## Statistical analysis

We performed all statistical analyses using the R statistical software (R Core Team 2022). We used linear mixed models (LMMs) in the lmer R package (Bates et al. 2015) to test for the association between chick body condition at hatching and the proportion of normal spermatozoa in the father's sperm. We included the proportion of normal spermatozoa, the rank of the chick (i.e., A- or B-chicks), their two-way interaction, as well as the year of sampling as fixed effects. The identity of the clutch was included as a random effect. We used linear models to test for the association between the proportion of normal spermatozoa in the father's sperm and post-hatching traits in A-chicks (i.e., body condition at the age of 10 days, mass growth between day 0 and day 10, and between day 10 and day 25, and maximum body mass before fledging). We included the proportion of normal spermatozoa and the sex of the chicks as fixed effects, because sexual dimorphism develops after hatching (Merkling et al. 2012). In LMMs, effects were tested via the Satterthwaite approximations for degrees of freedom for F-tests using the lmerTest package (Kuznetsova et al. 2017), and non-significant terms were backward dropped using a stepwise elimination procedure. Normality and homoscedasticity of the residuals of the models were checked graphically (Zuur et al. 2009).

## Results

Chick condition at hatching was related to the interaction between the proportion of normal spermatozoa and chick rank ($F_{1,25} = 8.10, P=0.009$; Fig. S1). This interaction was due to a decrease in the difference in body condition between A- and B-chick siblings with increasing proportion of normal spermatozoa ($\beta \pm SE = -7.98 \pm 2.68$; $F_{1,22} = 8.86, P=0.007$; Fig. 1). Neither in A-chicks, nor in B-chicks, condition at hatching varied with the proportion of normal spermatozoa (A-chicks: $\beta \pm SE = -3.56 \pm 2.98, F_{1,26} = 1.43, P=0.24$, and in B-chicks: $\beta \pm SE = 2.23 \pm 3.46$; $F_{1,22} = 0.41, P=0.53$; Fig. S1). The chicks tended to be in better condition at hatching in 2018 than in 2017 ($\beta \pm SE = 1.93 \pm 1.04$; $F_{1,27} = 3.43, P=0.075$).

In A-chicks, body mass growth rate over the first 10 days after hatching and chick condition at day 10 post-hatch were positively related to the proportion of normal spermatozoa ($\beta \pm SE = 8.55 \pm 3.38, F_{1,13} = 6.40, P=0.025$

and $\beta \pm SE = 72.89 \pm 22.72, F_{1,13} = 10.29, P=0.007$, respectively; Fig. 2a, b). Similarly, in A-chicks, the maximum body mass reached within the first 35 days after hatching increased with the proportion of normal spermatozoa ($\beta \pm SE = 119.99 \pm 31.57, F_{1,10} = 14.44, P=0.003$; Fig. 3). In contrast, the body mass growth rate between the age of 10 and 25 days did not vary with the proportion of normal spermatozoa ($\beta \pm SE = 1.27 \pm 4.29, F_{1,11} = 0.09, P=0.77$). Neither chick condition at day 10 post-hatch, nor body mass growth rate over the first 10 days or between day 10 and day 25 post-hatch, varied with the sex of the chicks ($\beta \pm SE = -11.67 \pm 8.59, F_{1,12} = 1.84, P=0.20, \beta \pm SE = -0.35 \pm 1.37, F_{1,12} = 0.065, P=0.80$ and $\beta \pm SE = 1.42 \pm 1.30, F_{1,11} = 1.19, P=0.30$). However, the maximum body mass reached within the first 35 days was higher in males than females ($431.9 \pm 16.3$ g and $406.3 \pm 8.9$ g; $\beta \pm SE = 30.98 \pm 11.50, F_{1,10} = 7.26, P=0.023$).

## Discussion

We investigated whether the proportion of normal spermatozoa was associated with offspring performance in a genetically monogamous seabird, the black-legged Kittiwake. Our results showed that this association varied over chick development.

At hatching, the difference in body condition between the A- and B-siblings decreased with increasing proportion of normal spermatozoa in the father's sperm. In Kittiwakes, A-chicks are larger and heavier than their sibling (Gill et al. 2002; Benowitz-Fredericks et al. 2013). Like in many other facultative siblicidal species (Morandini and Ferrer 2015), this mass and size difference between siblings leads to an intense chick competition, that often results in the death of the younger chick (White et al. 2010; Merkling et al. 2014). In these facultative siblicidal species, parents are expected to reduce the level of sibling competition when conditions for breeding are good, in order to increase the survival of both chicks (Slagsvold et al. 1984; Roulin et al. 2012; Muller and Groothuis 2013). For instance, female Kittiwakes seem to strategically reduce sibling competition, via the manipulation of androgen levels in eggs, when environmental conditions are good (Benowitz-Fredericks et al. 2013; Merkling et al. 2016). According to this hypothesis, the reduced asymmetry in body condition between siblings when the proportion of normal spermatozoa in the father's sperm is elevated may be a parental strategy to reduce the likelihood of siblicide when the father is of higher quality. In many bird species, chick condition at hatching is mainly determined by egg size (Hipfner and Gaston 1999; Reed et al. 1999; Styrsky et al. 1999; Krist 2011), which is closely related to the quantity of yolk and albumen deposited
<figure><img src="image_3.png" /><figcaption>**Fig. 1** Difference in body condition at hatching between A- and B-chicks in relation to the proportion of normal spermatozoa in the father's sperm. The line represents the linear trend between the two variables and the shaded area represents the 95% confidence interval</figcaption></figure>

by the female in eggs (Parsons 1976; Christians 2002). Accordingly, in our dataset, chick condition at hatching was strongly correlated with egg volume (Pearson's correlation test: *r* = 0.76, *P* < 0.0001). Therefore, the intra-brood difference in egg size - like the intra-brood difference in hatching body condition - decreased with increasing proportion of normal spermatozoa (linear models: F₁,₂₉ = 6.28, *P* = 0.018, β ± SE = -6.01 ± 2.40; Fig. S2). This result suggests that females' allocation into eggs may be the main driver of the association between sperm morphology and the difference

in hatching body condition between siblings. It further suggests that females might strategically adjust egg size to pre- or post-mating phenotypic cues correlated with their partner's sperm quality. Studies are needed to ascertain the existence of this maternal strategy and investigate its fitness benefits.

After hatching, A-chicks sired by males with higher proportion of normal spermatozoa grew faster and reached higher body condition at 10 days compared to A-chick sired by males with lower proportion of normal spermatozoa. In
<figure><img src="image_4.png" /><figcaption>**Fig. 2 (a)** Body mass growth rate between hatching and 10 days post-hatch and (b) body condition at 10 days post-hatch in A-chicks in relation to the proportion of normal spermatozoa in the father's sperm.</figcaption></figure>

The line represents the linear trend between the two variables, and the shaded area represents the 95% confidence interval

<figure><img src="image_5.png" /><figcaption>**Fig. 3** Maximum body mass before fledging in A-chicks in relation to the proportion of normal spermatozoa in the father's sperm. The line represents the linear trend between the two variables, and the shaded area represents the 95% confidence interval. One chick reached the maximum body mass at the age of 25 days (diamond point), five chicks reached the maximum body mass at the age of 30 days (round points) and seven chicks reached the maximum body mass at the age of 35 days (triangle points)</figcaption></figure>

addition, although they did not grow significantly faster between day 10 and day 25 post-hatch, they reached a higher maximum body mass before fledging. In our study, chicks were cross-fostered just after hatching suggesting that these results are not explained by differential parental care during chick development (e.g., by males with a higher proportion of normal spermatozoa providing better

parental care). In addition, because siblings were not cross-fostered together in the same nest, these results may not be explained by limited sibling competition when sperm quality is higher (i.e., the difference in body mass between the A-chick and its foster sibling did not vary with the sperm morphology of the A-chick's father; Spearman correlation test: *r* = -13, *P*=0.63; Fig. S3). Rather, the faster growth of A-chicks sired by males with higher proportion of normal spermatozoa may be explained by sperm quality, or any of its pre-hatching correlates, shaping chick growth and condition, once the time-limited effect of egg mass on chick condition vanishes (Smith and Bruun 1998; Bize et al. 2002). The mechanisms by which sperm morphology may affect offspring performance are poorly understood (Marshall 2015). However, sperm morphology is known to be associated with factors that can influence offspring performance, such as genetic and epigenetic variations (Ray et al. 2017), or the composition of the ejaculate (De Lazari et al. 2019).

The consequences of higher hatching condition, faster growth during the early nestling phase or higher peak mass reached before fledging on overall individual fitness are unknown in Kittiwakes. To the best of our knowledge, only faster chick growth during the linear growth phase has been shown to be associated with higher probability of recruitment in the colony (Coulson and Porter 1985; Vincenzi et al. 2015). However, a meta-analysis revealed that, in birds, larger offspring, both at hatching or at fledging, have higher survival (Ronget et al. 2018). In addition, while maximum chick mass reached before fledging has been poorly studied, it is suggested to be an adaptive insurance against starvation during periods of low parental provisioning or for later use
when energy requirements are increased (Lack 1968; Reid et al. 2000). Thus, in the common tern (*Sterna hirundo*), chicks that reach a higher peak mass before fledging have higher post-fledging survival (Ludwigs and Becker 2006).

In conclusion, although the selective pressures on sperm morphology are suggested to be relaxed in genetically monogamous species due to the absence of sperm competition (van der Horst and Maree 2014), the covariation between the proportion of normal spermatozoa and offspring performance in Kittiwakes indicates the potential for sperm quality to be under natural selection. In addition, this covariation may act as a selective pressure influencing the evolution of maternal strategies. In Kittiwakes, partners copulate long before the fertile period, but these early copulations are often followed by the female rejecting sperm (Wagner et al. 2004). Because prolonged sperm storage in the female tract impairs embryo development (White et al. 2008), sperm rejection has been suggested to be a female strategy to limit egg fertilization by poor quality old sperm (Wagner et al. 2004; Pineaux et al. 2019). Clearly, the effect of sperm quality on the biology of genetically monogamous species should not be overlooked.

**Supplementary Information** The online version contains supplementary material available at https://doi.org/10.1007/s00265-024-03540-w.

**Acknowledgements** We thank Shannon Whelan, Lucie Abolivier, Thomas Pagnon, Camille Toscani, Tony Rinaud, Célia Maillotte and Eléonore Lefebvre for their help in the field. We thank Guillaume Lespagnol, Julie Bosca and Lucie DiGesu for their help in sperm analyses.

**Funding** The study was financed by grants from the French Polar Institute (IPEV Programme 1162 SexCoMonArc2 to SL) and from the Fondation Fyssen (to SL). This study is part of the Laboratoire d'Excellence (LABEX) entitled TULIP (ANR-10-LABX-41). Open access funding provided by Université Toulouse III - Paul Sabatier.

**Data availability** Data are available at DOI https://doi.org/10.17605/OSF.IO/K2ST4.

**Declarations**

**Ethical approval** This experiment was conducted under the approval of the USGS Alaska Science Centre Animal Care and Use Committee, in accordance with US law and under permits from the US Fish and Wildlife Service and the State of Alaska. All applicable international, national, and institutional guidelines for the use of animals were followed.

**Conflict of interest** The authors have no relevant financial or non-financial interests to disclose.

**Open Access** This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format,

as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

**References**

Auger J (2010) Assessing human sperm morphology: top models, underdogs or biometrics? Asian J Androl 12:36–46. https://doi.org/10.1038/aja.2009.8

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

Benowitz-Fredericks ZM, Kitaysky AS, Welcker J, Hatch SA (2013) Effects of food availability on yolk androgen deposition in the black-legged Kittiwake (*Rissa tridactyla*), a seabird with facultative brood reduction. PLoS ONE 8:e62949

Bize P, Roulin A, Richner H (2002) Covariation between egg size and rearing condition determines offspring quality: an experiment with the alpine swift. Oecologia 132:231–234. https://doi.org/10.1007/s00442-002-0980-y

Blount JD, Møller AP, Houston DC (2001) Antioxidants, showy males and sperm quality. Ecol Lett 4:393–396. https://doi.org/10.1046/j.1461-0248.2001.00255.x

Boissonnas CC, Abdalaoui HE, Haelewyn V, Fauque P, Dupont JM, Gut I, Vaiman D, Jouannet P, Tost J, Jammes H (2010) Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 18:73–80. https://doi.org/10.1038/ejhg.2009.117

Burley N (1988) The differential-allocation hypothesis - an experimental test. Am Nat 132:611–628

Cam E, Aubry L (2011) Early development, recruitment and life history trajectory in long-lived birds. J Ornithol 152:187–201

Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26. https://doi.org/10.1017/S1464793101005784

Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org

Coulson JC, Porter JM (1985) Reproductive success of the Kittiwake *Rissa tridactyla*: the roles of clutch size, chick growth rates and parental quality. Ibis 127:450–466

Daneshmandpour Y, Bahmanpour Z, Hamzeiy H, Mazaheri Moghadam M, Mazaheri Moghaddam M, Khademi B, Sakhinia E (2020) MicroRNAs association with azoospermia, oligospermia, asthenozoospermia, and teratozoospermia: a systematic review. J Assist Reprod Genet 37:763–775. https://doi.org/10.1007/s10815-019-01674-9

De Lazari FL, Sontag ER, Schneider A, Moura AAA, Vasconcelos FR, Nagano CS, Mattos RC, Jobim MIM, Bustamante-Filho IC (2019) Seminal plasma proteins and their relationship with sperm motility and morphology in boars. Andrologia 51:e13222. https://doi.org/10.1111/and.13222

De Vos A, Van de Velde H, Joris H, Verheyen G, Devroey P, Van Steirteghem A (2003) Influence of individual sperm morphology on fertilization, embryo morphology, and pregnancy outcome of
intracytoplasmic sperm injection. Fertil Steril 79:42-48. https://doi.org/10.1016/S0015-0282(02)04571-5

Evans JP, Lymbery RA, Wiid KS, Rahman MM, Gasparini C (2017) Sperm as moderators of environmentally induced paternal effects in a livebearing fish. Biol Lett 13:20170087. https://doi.org/10.1098/rsbl.2017.0087

Fernández-Gonzalez R, Moreira PN, Pérez-Crespo M et al (2008) Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol Reprod 78:761-772. https://doi.org/10.1095/biolrep rod.107.065623

Firman R, Simmons LW (2009) Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64:1245-1256. https://doi.org/10.1111/j. 1558-5646.2009.00894.x

Firman RC, Simmons LW (2011) Experimental evolution of sperm competitiveness in a mammal. BMC Evol Biol 11:19. https://doi. org/10.1186/1471-2148-11-19

Fitzpatrick JL, Lüpold S (2014) Sexual selection and the evolution of sperm quality. Mol Hum Reprod 20:1180-1189. https://doi.org/1 0.1093/molehr/gau067

Gasparini C, Dosselli R, Evans JP (2017) Sperm storage by males causes changes in sperm phenotype and influences the reproduc- tive fitness of males and their sons. Evol Lett 1:16-25. https://do i.org/10.1002/evl3.2

Gebhardt-Henrich S, Richner H (1998) Causes of growth variation and its consequences for fitness. Oxf Ornithol Ser 8:324-339

Gill VA, Hatch SA (2002) Components of productivity in black-legged
kittiwakes *Rissa tridactyla*: response to supplemental feeding. J
Avian Biol 33:113-126. https://doi.org/10.1034/j.1600-048X.20
02.330201.x

Gill VA, Hatch SA, Lanctot RB (2002) Sensitivity of breeding param-
eters to food supply in black-legged Kittiwakes *Rissa tridactyla*.
Ibis 144:268-283

Helfenstein F, Tirard C, Etienne Danchin RHW (2004) Low frequency of extra-pair paternity and high frequency of adoption in black-legged Kittiwakes. Condor 106:149-155

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. https://doi.org/10.1111/j.1461-024 8.2009.01419.x

Hipfner JM, Gaston AJ (1999) The relationship between egg size and posthatching development in the thick-billed murre. Ecology 80:1289-1297. https://doi.org/10.2307/177075

Humann-Guilleminot S, Blévin P, Azou-Barré A, Yacoumas A, Gabri-
elsen GW, Chastel O, Helfenstein F (2018) Sperm collection in
Black-legged Kittiwakes and characterization of sperm velocity
and morphology. Avian Res 9:24. https://doi.org/10.1186/s4065
7-018-0117-6

Immler S, Calhim S, Birkhead TR (2008) Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538-1543. https://doi.org/10.1111/j.1558-5646.20 08.00393.x

Jacobs SR, Elliott K, Guigueno MF, Gaston AJ, Redman P, Speakman JR, Weber J-M (2012) Determining seabird body condition using nonlethal measures. Physiol Biochem Zool 85:85-95. https://doi .org/10.1086/663832

Koffler S, Meneses HM, Kleinert A, de MP, Jaffé R (2016) Competi-
tive males have higher quality sperm in a monogamous social
bee. BMC Evol Biol 16:195. https://doi.org/10.1186/s12862-01
6-0765-2

Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86:692-716. https://doi.org/10.1111/j.1469-185X.2010. 00166.x

Kuznetsova A, Brockhoff PB, Christensen RHB (2017) ImerTest pack-
age: tests in linear mixed effects models. J Stat Softw 82:1-26

Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

Leclaire S, Bourret V, Wagner RH, Hatch SA, Helfenstein F, Chastel O, Danchin E (2011) Behavioral and physiological responses to male handicap in chick-rearing black-legged Kittiwakes. Behav Ecol 22:1156-1165. https://doi.org/10.1093/beheco/arr149

Ludwigs J-D, Becker P (2006) Individual quality and recruitment in the Common Tern, *Sterna hirundo*. Acta Zool Sin 52:96-100

Lüpold S, Pitnick S (2018) Sperm form and function: what do we know about the role of sexual selection? Reproduction 155:R229-R243. https://doi.org/10.1530/REP-17-0536

Lüpold S, de Boer RA, Evans JP, Tomkins JL, Fitzpatrick JL (2020) How sperm competition shapes the evolution of testes and sperm: a meta-analysis. Phil Trans R Soc B 375:20200064. https://doi.or g/10.1098/rstb.2020.0064

Macartney EL, Morrison K, Snook RR, Lagisz M, Nakagawa S (2024) Intra-specific correlations between ejaculate traits and competitive fertilization success: a meta-analysis across species and fertilization modes. Evolution 78:497-510. https://doi.org/10.1093/ evolut/qpad229

Marshall DJ (2015) Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects. J Exp Biol 218:107-113. https://doi.org/10.1242/jeb.106427

Mehrpvarvar B, Chashmniai S, Nobakht F, Amini M, Javidi A, Minai-
Tehrani A, Arjmand B, Gilany K (2020) Metabolic profiling of
seminal plasma from teratozoospermia patients. J Pharm Biomed
Anal 178:112903. https://doi.org/10.1016/j.jpba.2019.112903

Merkling T, Leclaire S, Danchin E, Lhuillier E, Wagner RH, White J, Hatch SA, Blanchard P (2012) Food availability and offspring sex in a monogamous seabird: insights from an experimental approach. Behav Ecol 23:751-758. https://doi.org/10.1093/behe co/ars023

Merkling T, Agdere L, Albert E, Durieux R, Hatch SA, Danchin E, Blanchard P (2014) Is natural hatching asynchrony optimal? An experimental investigation of sibling competition patterns in a facultatively siblicidal seabird. Behav Ecol Sociobiol 68:309-319. https://doi.org/10.1007/s00265-013-1646-y

Merkling T, Perrot C, Helfenstein F, Ferdy J-B, Gaillard L, Lefol E, Voisin E, Hatch SA, Danchin E, Blanchard P (2016) Maternal effects as drivers of sibling competition in a parent-offspring conflict context? An experimental test. Ecol Evol 6:3699-3710

Morandini V, Ferrer M (2015) Sibling aggression and brood reduction: a review. Ethol Ecol Evol 27:2-16. https://doi.org/10.1080/0394 9370.2014.880161

Morgan HL, Watkins AJ (2020) The influence of seminal plasma on offspring development and health. Semin Cell Dev Biol 97:131-137. https://doi.org/10.1016/j.semcdb.2019.06.008

Muller M, Groothuis TGG (2013) Within-clutch variation in yolk tes-
tosterone as an adaptive maternal effect to modulate avian sib-
ling competition: evidence from a comparative study. Am Nat
181:125-136. https://doi.org/10.1086/668601

Nusbaumer D, Da Cunha LM, Wedekind C (2019) Sperm cryopreser-
vation reduces offspring growth. Proc R Soc B 286:20191644.
https://doi.org/10.1098/rspb.2019.1644

Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525-567. https://doi.org/10.1111/j.1469-185X.1970.tb01176.x

Parsons J (1976) Factors determining the number and size of eggs laid by the herring gull. Condor 78:481-492. https://doi.org/10.2307/1367097

Peng Y, Zhao W, Qu F, Jing J, Hu Y, Liu Y, Ding Z (2019) Proteomic alterations underlie an association with teratozoospermia in obese mice sperm. Reprod Biol Endocrinol 17:82. https://doi.org/10.1186/s12958-019-0530-7

Pineaux M, Blanchard P, Danchin É, Hatch SA, Helfenstein F, Mulard H, White J, Leclaire S, Wagner RH (2019) Behavioural avoidance
of sperm ageing depends on genetic similarity of mates in a
monogamous seabird. *Biol J Linn Soc* 128:170–180

Pineaux M, Merkling T, Danchin É, Hatch SA, Duneau D, Blanchard P, Leclaire S (2020) Sex and hatching order modulate the association between MHC-II diversity and fitness in early-life stages of a wild seabird. *Mol Ecol* 29:3316–3329. https://doi.org/10.1111/mec.15551

Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm Biology: an evolutionary perspective. Academic, London, pp 207–245

Pukazhenti BS, Wildt DE, Howard JG (2001) The phenomenon and significance of teratospermia in felids. *J Reprod Fertil Suppl* 57:423–433

Ray Pf, Toure A, Metzler-Guillemain C, Mitchell MJ, Arnoult C, Cout-
ton C (2017) Genetic abnormalities leading to qualitative defects
of sperm morphology or function. *Clin Genet* 91:217–232. https:
//doi.org/10.1111/cge.12905

Reed WL, Turner AM, Sotherland PR (1999) Consequences of egg-
size variation in the red-winged blackbird. *Auk* 116:549–552.
https://doi.org/10.2307/4089390

Reid K, Prince PA, Croxall JP (2000) Fly or die: the role of fat stores in the growth and development of Grey-headed Albatross *Diomedea chrysostoma* chicks. *Ibis* 142:188–198. https://doi.org/10.1111/j. 1474-919X.2000.tb04858.x

Ronget V, Gaillard J-M, Coulson T, Garratt M, Gueyffier F, Lega J-C, Lemaître JF (2018) Causes and consequences of variation in off-spring body mass: meta-analyses in birds and mammals. *Biol Rev* 93:1–27. https://doi.org/10.1111/brv.12329

Roulin A, Dreiss AN, Royle NJ, Smiseth PT (2012) Sibling competi-
tion and cooperation over parental care. In: Royle NJ, Smiseth
PT, Kölliker M (eds) The evolution of parental care. Oxford Uni-
versity Press, Oxford, pp 133–149

Simmons LW, Fitzpatrick JL (2012) Sperm wars and the evolution of male fertility. *Reproduction* 144:519–534. https://doi.org/10.1530/REP-12-0285

Simmons LW, Lovegrove M (2019) Nongenetic paternal effects via seminal fluid. *Evol Lett* 3:403–411. https://doi.org/10.1002/evl3.124

Slagsvold T, Sandvik J, Rofstad G, Lorentsen Ö, Husby M (1984) On the adaptive value of intraclutch egg-size variation in birds. *Auk* 101:685–697

Smith HG, Bruun M (1998) The effect of egg size and habitat on star-
ling nestling growth and survival. *Oecologia* 115:59–63. https://d
oi.org/10.1007/s004420050491

Styrsky JD, Eckerle KP, Thompson CF (1999) Fitness-related consequences of egg mass in nestling house wrens. Proc R Soc Lond B 266:1253–1258. https://doi.org/10.1098/rspb.1999.0771

van der Horst G, Maree L (2014) Sperm form and function in the absence of sperm competition: absence of sperm competition. Mol Reprod Dev 81:204–216. https://doi.org/10.1002/mrd.22277

Vincenzi S, Hatch S, Mangel M, Kitaysky A (2013) Food availability affects onset of reproduction in a long-lived seabird. Proc R Soc B 280:20130554. https://doi.org/10.1098/rspb.2013.0554

Vincenzi S, Hatch S, Merkling T, Kitaysky AS (2015) Carry-over effects of food supplementation on recruitment and breeding performance of long-lived seabirds. Proc R Soc B 282:20150762. https://doi.org/10.1098/rspb.2015.0762

Wagner RH, Helfenstein F, Danchin E (2004) Female choice of young sperm in a genetically monogamous bird. Proc R Soc Lond B 271:S134–S137. https://doi.org/10.1098/rsbl.2003.0142

Watkins AJ, Rubini E, Hosier ED, Morgan HL (2020) Paternal programming of offspring health. Early Hum Dev 150:105185. https://doi.org/10.1016/j.earlhumdev.2020.105185

White J, Wagner RH, Helfenstein F, Hatch SA, Mulard H, Naves LC, Danchin E (2008) Multiple deleterious effects of experimentally aged sperm in a monogamous bird. P Natl Acad Sci USA 105:13947–13952. https://doi.org/10.1073/pnas.0803067105

White J, Leclaire S, Kriloff M, Mulard H, Hatch SA, Danchin E (2010) Sustained increase in food supplies reduces broodmate aggression in black-legged kittiwakes. *Anim Behav* 79:1095–1100

Wigby S, Chapman T (2004) Sperm competition. Curr Biol 14:R100–R103. https://doi.org/10.1016/j.ympev.2004.01.013

Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

**Publisher's note** Springer Nature remains neutral with regard to juris-
dictional claims in published maps and institutional affiliations.