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Animal experiment

We used captive bred red junglefowl from our facility at the University of Groningen, The Netherlands, which is an outbred population of wild caught birds coming originally from Asia. All males displayed the species-specific calls, much shorter than those from domestic birds, and most birds still moulted their neck feathers in autumn. We performed a power analysis based on data of an earlier experiment where we found an effect of dominance on egg mass. This revealed (power 0.8, alpha 0.05) the sample size we used for the number of pairs. Since we needed chicks of both sexes from each pair, we aimed for at least 3–4 eggs from each pair that would successfully hatch, taking into account the level of hatching success in earlier experiments using this species. The welfare of all birds was assessed on a daily basis throughout the experiment. The animal observations were done for 30 minutes during the male-male confrontations and before and thereafter all birds were checked two times a day. All handling and treatment of animals were carried out by experienced scientists and animal caretakers with a licence to perform animal experiments. All experimental procedures were carried out according to the regulation of Dutch law for laboratory animals and approved by the animal experimentation committee of the University of Groningen the Netherlands (licence DEC 6710 C in 2014).

Experiment 1: Social status and testosterone in blood plasma and ejaculates

Experimental design

To determine T concentration of males of different social status, we selected 10 males (±2.5 years old) on the basis of comb size and body mass such that 5 potentially dominant males had a larger comb size and a larger body size than 5 subordinate chickens (see SI Section 1). Before the experiment, all 10 males were housed in the multi-male group. The predicted winners (large combed and heavy males) and predicted loser (small comb and light males) were allocated to one of 10 identical aviaries ((1.5 by 4 by 2 m) (w × l × h)) four days before the experiment, containing ad lib food, grit and water. After 4 days, randomly chosen small combed males were introduced into the cages of the predicted winners. In the first 30 minutes after introduction each pair was observed to determine the dominance relationship between the males. Dominance was quickly established within 15 minutes and often within 5 minutes. Dominance was determined by observing aggressive approaches (raised neck feathers), lateral display, crowing, and overt aggression, and by withdrawal and freezing as a reaction of the subordinate males. Twenty-four hours later an ejaculate sample and a blood sample were obtained in which T concentration were determined (see SI section 2, 3, and 6). Ejaculate samples were weighed before hormone analyses. As expected, all the preselected winners were dominant over the preselected losers. Male biometry is outlined in Tables A and B of the SI section.

Experiment 2: Effects of testosterone enriched ejaculate

Experimental design

Since winner males had lower T concentration in their ejaculates than loser males, we investigated whether ejaculate T concentration affected female reproductive investment. Prior to the experiment, the chickens were housed in all female or all male flocks. Male and females were about one year old (8–10 month) and sexually naïve at the start of this experiment. Hens were assigned to a treatment condition such that there were no differences in body mass between the control and treatment groups (see Table 1). Thirteen potentially dominant and subordinate males were selected in 2014 and twelve pairs in 2015 from our stock and housed in identical aviaries (see above). The criteria for potential dominant males was based on their body mass and comb size as above. Male biometry was determined before the first and the second part of experiment 2. Each male was housed in a triplet cage, i.e. the male was placed in the middle of three identical aviaries, between two females that were physically but not visually separated from the male by wire mesh. In order to strengthen the perceived attractiveness of the males in such a triplet, each male was confronted with an intruder male for 15 minutes (one day after the initial housing event) and left to exert its dominance over the intruder in full view of the females. This procedure was repeated every week during the entire experiment. This procedure was carefully monitored for (1) animal welfare reasons and (2) to check whether the resident male indeed was dominant over the intruder, which was always the case. The males in the middle of the triplet were the ejaculate donors for the insemination procedure. Each female in a triplet was either inseminated with a T enriched ejaculate (TE) or received the control treatment (CE) every other day (for treatment details on T concentration see below). Females were allowed to lay a clutch (clutch number 1, autumn 2014) and we recorded female reproductive investment (clutch size, egg mass, and clutch mass). Eggs were collected every afternoon and individually marked with non-toxic ink and stored at room temperature (see SI section 5). Directly after clutch completion, the treatment was reversed and the same variables were recorded (clutch number 2). After the second clutch, the treatment was reversed again. Females were allowed to produce a third clutch (number 3). Eggs from this clutch were collected and artificially incubated in order to assess whether there were any effects of the treatment on offspring growth and behaviour. Newly hatched chicks from clutch number 3 were housed in cages (100 cm × 100 cm × 100 cm) in our inside facility under LD 14:10 h, 60% relative humidity, and a room temperature of 24 °C. Chicks were randomly housed in groups of 5 to 10 (average 8) according to laying date and mixed across treatments (and sex). Each cage was fitted with a red heat light. Food and water were provided in ad libitum quantities. Individual birds were fitted with a rubber colour band directly after hatching and at three weeks old they received a numbered metal wing clip through the patagium. At this age, the sex of the chicks could be determined based on the size of the comb and the feather colour in the neck and chest region.

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The experiment was repeated the following spring (2015). The hens of the TE treatment in the previous group were switched to the CE treatment and vice versa (see Fig. 5). All females remained matched to the same males. Females treated with TE and CE were allowed to produce a clutch again (clutch number 4). After clutch completion females were left to recuperate for one week after which treatment was reversed once more and the hens were left to produce a fifth clutch. The eggs of clutch 4 and 5 were collected for the analyses of yolk T and androstenedione (A4) deposition (see SI section 3 and 6). This repetition involved 24 of the original 26 hens from the experiment in 2014 (2 hens had died during the winter). The overall design is schematically illustrated in Fig. 5. Figure 5 Schematic representation of experiment 2. In total hens produced 5 clutches in either the TCTCT condition or CTCTC condition where T stands for insemination with testosterone enriched ejaculate and C for insemination with control ejaculate. Time runs from left to right. The third clutch is not included because it was used to determine offspring growth and behaviour. Full size image

Ejaculate treatment protocol

After housing males and females in triplets, we collected fresh ejaculates from all the dominant males every other day. Ejaculates were pooled in a vial (±4 ml), and then half of the ejaculate was enriched with 0.5 ng testosterone suspended in 30 µl sesame oil per 0.17 ml ejaculate (TE). This increased the relative low testosterone concentration of the ejaculate of winners (see experiment 1) from 0.96 to 3.31 ng/ml (total amount was 0.66 ng hormone, as 0.2 ml was used for insemination represent the ejaculate volume of normal copulation) which is within the physiological range of the testosterone concentration in the ejaculate of losers (close to the average plus 2 times the standard deviation of the mean). The other half of the females received 0.17 ml ejaculate mixed with 30 µl sesame oil only (CE). Because of the addition of the sesame oil, control birds received a slightly lower T concentration, from 0.96 to 0.82 ng/ml, than that of dominant male ejaculates (total amount per insemination: 0.16 ng). To maintain the ejaculates at body temperature (±42 °C for red junglefowl), vials were kept in a water bath with the same temperature until artificial insemination (directly after mixing), which was between 60–120 minutes after ejaculate collection. For artificial insemination, hens were caught and held in an inverted position in which the muscle around the ischium was gently massaged. Once the upper and lower lip of the cloaca opened, a syringe was inserted, and females received 0.2 ml of either T enriched ejaculate mix or the control mix. Each female was inseminated every other day for three weeks or until clutch completion. Inseminations took no longer than 3 minutes and were habitually performed between 10.00, and 12.00 am after most hens had laid an egg.

Behavioural tests

We tested the chicks in two behavioural paradigms: (1) a food competition test (age 4–8 days) and (2) a tonic immobility test (age 21 days), see also SI section 4. In the food competition test (n = 59) we tested both same-sex and opposite-sex dyads with 30 chicks from T enriched ejaculate treated mothers and 29 chicks from control mothers. We used the 59 survivors for the TI test and for the analysis of growth until five weeks of age. For the competition test we marked control chicks such that they could be recognized during the video analyses. In each competitive test, a pair of focal birds (two individuals from different treatments) were placed in a circular arena (diameter = 80 cm) behind a wire barrier. Then a mealworm (Tenebrio molitor), a very attractive food item for the chicks, was placed on the other side of the barrier. As soon as both chicks showed interest, the barrier was removed and they were left to compete for the item which occurred in all tests. The test ended when the meal worm was eaten. For each pair 5 such trails were conducted. The total number of mealworms obtained by each individual was summed over the five trials. We also determined which chick ate most of the mealworms over the five trials. At the age of three weeks we performed a tonic immobility test58,59. The tonic immobility test was performed blindly with respect to sex and treatment. The tests were performed in the same room where the chicks were housed in, to avoid additive effects of a novel environment. Chicks were placed on a table in the middle of the room and held on their back for approximately 10 seconds, then the researcher slowly retracted his hand and the time it took for the chick to be fully upright again was recorded. All animals were tested in five consecutive trials.

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Body mass was determined directly after hatching and then every week until they were 5 weeks old. After five weeks, all chicks were moved to a single large aviary.

Statistical analyses

The data of differences between winners and losers in plasma and ejaculate T concentration, body mass, comb size and the comb size relative to body mass were tested with paired t-tests. The effect of treatment on egg mass (data of 2014 and 2015 were pooled) was tested using linear mixed models, with each egg nested in clutch and clutch nested in mother as a random effect. Models included clutch number (order in which the clutches were produced), treatment and the interaction between clutch number and treatment as fixed effects. Post-hoc tests were fitted for differences within clutches using linear mixed models with each egg nested in mother as a random effect. For effects of treatment on other reproductive variables (clutch size, clutch mass and hormone concentration), the data were analysed using linear mixed models with clutch nested in hen as a random effect. For the egg components: albumin, shell, yolk mass and hormone concentration, the analysis was only conducted on data from 2015 (no data was collected in 2014), using clutch number 4 and 5. The linear mixed models included clutch, treatment and the interaction between clutch and treatment as fixed effects. In the offspring growth analysis, the dependent factor was the body mass of chicks (gram) at six different time points from the day of hatching until 5 weeks of age. The data were analysed using linear mixed models with treatment, sex, age and the interaction between treatment, sex and age, as fixed effects and chick nested within mother as a random effect. A post-hoc test for body mass at 5 weeks after hatching was fitted using a linear mixed model with treatment, sex, and the interaction between treatment and sex as fixed effects and chick nested within mother as a random effect. The effect of treatment on tonic immobility was tested using a linear mixed model, with each trial (5 times) nested in chick as a random effect. Models included treatment, sex and the interaction between treatment and sex as fixed effects. A post-hoc test for the duration of tonic immobility based on the sex was fitted using a linear mixed model, with each trial nested in chicks as a random effect and treatment as fixed effect. The residuals of the mixed models were checked for normality (see Supplementary Data Set). The effect of treatment on the performance in the competition test between the chicks of the two treatments was analysed as follows: we first fitted a univariate analysis of variance on the difference within each chick pair, in the number of mealworms eaten, separately for same-sex and opposite-sex trials with the difference in body mass (TE-CE) as a covariate, and calculated whether the intercept differed from 0. Subsequently we tested in same-sex and opposite-sex competitive trials whether the number of birds that ate the majority of the mealworms offered, differed between the treatments using proportion tests. All statistical analyses were performed with SPSS23. and the models have been tested for normality using their residual values (see Supplementary Data Set).

nature.com - Ejaculate testosterone levels affect maternal investment in red ... - Nature

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