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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2020 Mar 4;287(1922):20192578. doi: 10.1098/rspb.2019.2578

Mate selection based on labile traits affects short-term fitness in a long-lived seabird

Erick González-Medina 1,2,✉, José Alfredo Castillo-Guerrero 3, José A Masero 2, Guillermo Fernández 4
PMCID: PMC7126066  PMID: 32126956

Abstract

In long-lived monogamous social species, partner compatibility can play a crucial role in reproductive success. We evaluated assortative mating based on body condition (plasma triglyceride concentration), diet (δ15N), and foraging habitat (δ13C) in the blue-footed booby Sula nebouxii, a long-lived monogamous seabird. We investigated the effects of assortative mating (sum of triglycerides in a pair) and asymmetry within pairs (residuals from regression of female–male triglycerides) on reproductive performance and offspring growth (alkaline phosphatase, ALP). We found that strong assortative mating determined by body condition and diet seemed to be related to a signalling mechanism (nutritional state). This mating pattern had a substantial effect on the breeding parameters and influenced offspring ALP. Within-pair asymmetry did not influence any reproductive parameters, but the ALP of offspring was related to the within-pair relative female condition. Overall, our results indicate that individuals seek the best possible match to maximize their breeding investment and/or individuals are limited in their mate options by their current body condition, which has consequences for offspring fitness in the short term. Our findings show that assortative mating based on body condition produces notable variation in the joint condition of the pair, which determines their breeding success.

Keywords: assortative mating, labile traits, triglyceride, stable isotopes, alkaline phosphatase

1. Introduction

In socially monogamous breeding systems, partner compatibility plays a crucial role in reproductive success [1,2]. In birds and fishes, when compatibility (e.g. behavioural or physiological compatibility) is higher, reproductive success and offspring condition are higher [2–4]. Assortative mating among animals is an extended pair-selection mechanism [5] and is defined as individuals of similar phenotype or quality mating more frequently than expected by random sorting [6]. In species with biparental care, both sexes actively select their partners [7,8], and high-quality individuals are expected to be more selective than low-quality individuals [9]. Assortative mating studies have focused mainly on the use of fixed traits (e.g. plumage colouration or tail length) in mate selection, but recent research has reported the use of labile or dynamic traits that may vary with environmental conditions (e.g. behaviour, body condition, diet) [5,10–13]. However, the underlying processes that drive these patterns are often poorly understood, and there is little evidence about the resulting fitness consequences [14,15]. It is of interest to investigate how mate selection based on non-fixed traits affects reproductive performance and to identify the resulting fitness consequences.

The effects of mating between individuals of different ‘quality’ have been investigated broadly. In birds, for example, females that mate with ‘low-quality’ males have delayed laying dates [16], increased circulating corticosterone concentrations (indicating increased stress) [17], decreased time spent at the nest, decreased egg size [18,19], and increased probability of having extra-pair offspring [20] relative to females that mate with ‘high-quality’ mates. This evidence supports the idea that if a partner does not have an equitable ‘quality’, adjustments can be made in reproductive investment and thus affect reproductive success. Therefore, the best strategy to find a partner is to find a mate with a similar or increased mating quality. Among pairs, there may also be a gradient of ‘asymmetries’ (wherein some partners are more similar than others). Such asymmetries can also influence partner compatibility and the reproductive investment of each partner [21]. To the best of our knowledge, no study has evaluated the consequences of assortative mating while considering the differences between and within pairs and the short-term fitness consequences.

Blue-footed boobies (BFBOs, Sula nebouxii) are socially monogamous long-lived seabirds with an extended biparental care period of up to six months [22] and a high annual divorce rate of up to 50% [23]. BFBOs evaluate their mates before and after pairing and can perform rapid adjustments of reproductive investment by using information from dynamic traits such as the colour of the feet [24–27]. This colour is a dynamic condition-dependent trait, the expression of which changes rapidly with fluctuations in nutritional status and body condition (in less than 48 h) [24,27]. For example, male foot colour influences female investment in eggs [27] and is associated with the body condition of their offspring [26]. This evidence could suggest that assortative mating in BFBOs is related to body condition, but to date, no study has explicitly analysed whether this species engages in assortative mating. In this study, we investigated whether assortative mating exists in BFBOs by considering three labile traits related to body condition, diet, and foraging habitat: plasma triglyceride concentration, δ15N, and δ13C, respectively. We also assessed whether the sum of triglyceride concentration (Sum-Trigls) of a pair and the asymmetry within a pair (regression residuals of the triglyceride concentrations of males versus females) affect reproductive performance (total egg volume, hatching success, and fledging success) or the potential growth rate of their offspring (measured as alkaline phosphatase (ALP) concentration).

Triglyceride concentration is positively associated with feeding, fat deposition, mass gain, and cell-mediated immune response [28–30] in either the short term [31] or over extended periods (e.g. weeks) [32]. Data for seabirds are scarce, but it has been shown that triglyceride concentration is correlated with body mass in storm petrels [29]. Additionally, some seabird studies indicated that triglyceride concentration was significantly increased before egg laying [33–35]. In our model species, body condition (size-corrected body mass) is correlated significantly with plasma triglyceride levels during the breeding season [19]. Given this relationship and that foot colour in BFBOs changes rapidly with body condition, it is reasonable to expect plasma triglyceride levels to vary with foot colour as they do in other bird species; for example, in the lesser kestrel, Falco naumanni, tarsal colouration changes with triglyceride concentration [36]. In addition, ALP concentration provides information on the body condition and growth of offspring [37,38]. Offspring ALP concentration is related to the quality of food a chick receives from parents [39] and to the chick's body condition (chicks with higher ALP concentrations in blood plasma have superior body conditions; [38,40]). Furthermore, the δ15N and δ13C values of seabirds can be used as proxies for their diet/trophic position and foraging habitat, respectively [41]. δ15N values generally increase with trophic level and are, therefore, used to estimate the trophic level of consumers [42], while δ13C values show higher enrichment in inshore species than in offshore species [43], providing insight into foraging regions and feeding preferences. Stable isotope values of whole blood samples of birds are useful for assessing the relationship between diet and nutritional condition because they reflect the diet assimilated over the previous three to four weeks [42,44].

Considering that there is an exchange of information between mates through the colour of the feet and that this colour reflects body condition [24–27], we expected assortative mating with respect to plasma triglyceride concentration. We expected positive relationships of plasma triglyceride concentration in each pair with reproductive performance and offspring growth rate. Moreover, as the degree of asymmetry in triglyceride concentration within pairs can influence reproductive performance, we predicted that pairs with more similar concentrations would have better reproductive performance than would those with less similar ones.

2. Material and methods

(a). Study population and general procedures

The fieldwork was conducted in a colony (3490 ± 440 reproductive pairs) of BFBOs located on the island Isla El Rancho (25°10′ N, 108°23′ W; 327 ha), which is less than 1 km from the northern mouth of Bahía Santa María-La Reforma, the largest coastal wetland in the state of Sinaloa, Mexico [45].

We visited the island for 5–6 consecutive days every two weeks between December and May (breeding season, 2011–2012). We randomly selected 23 pairs of BFBOs during the courtship period. BFBO pairs were individually marked with alphanumeric rings and monitored throughout the breeding season. During each visit, we checked every marked nest daily; thus, in most cases, we knew the precise hatching date and fledging success. We assumed that a chick fledged successfully when a bird with complete juvenile plumage left its nest and returned to it with clean feet. Laying date, clutch size, egg volume, laying and hatching order, number of hatching eggs, and fledglings (offspring that flew) were recorded. Eggs were measured with callipers (±0.1 mm), and egg volume (cm3) was calculated as the maximum length × maximum width2 × 0.51/1000 [46], a method previously used for this species [18]. The total egg volume per clutch was calculated as the sum of individual egg volumes in the clutch. We caught adults and chicks in their nests to collect blood samples (approx. 1.5 ml) from the brachial vein. Adults were sampled during courtship (number of pairs = 23) and the chick-rearing period (number of pairs = 21), and their offspring were sampled during the chick-rearing period (at 44.4 ± 8.2 days old, n = 27 chicks). Only blood samples obtained from adults during the courtship period were used because individuals select their partners during this period, and our interest was in pair selection and its potential short-term consequences. Adult blood samples obtained during the chick-rearing period were used only to corroborate if the pattern obtained during courtship was maintained during the breeding season (see electronic supplementary material, figure S1). Adult pairs were captured and bled on the same date but not always at the same time; chicks from the same nest were captured and bled on the same date and time. Samples were transferred to two polypropylene tubes (0.5 and 1 ml) without anticoagulant. In some cases, the collected blood volume was insufficient to measure all the variables. In that case, we prioritized metabolite analyses, so the sample size was decreased in the isotopic analyses. The time between capture and blood collection was always less than 15 min (9.6 ± 3.5 min on average). Adults and chicks were returned to their nests immediately after sampling (within less than 3 min). One of the tubes was centrifuged 2800 × g for 10 min for subsequent measurements of triglyceride and ALP concentrations in the plasma. The other tube was left untreated and used for isotopic analyses. All samples were maintained on ice in the field and then frozen in the laboratory at −20°C pending preparation for analysis.

(b). Triglyceride and alkaline phosphatase concentrations

Plasma concentrations of total triglycerides (triglycerides plus free glycerol) and ALP were assayed in a multiparameter chemistry analyser (Falcor 360; Menarini Diagnostics, Barcelona, Spain) with commercial kits (Menagent; Menarini Diagnostics). The analyser was calibrated with a commercial calibration kit (Menagent; Menarini Diagnostics), and control reference serum samples (Menagent; Menarini Diagnostics) were run together with plasma samples. Plasma concentrations of free glycerol were assayed via endpoint assay on a microplate spectrophotometer (BioTek, Winooski, VT, USA) using standard diagnostic kits and 400 µl flat-bottom microplates (Greiner Bio-One, Germany). The commercial kits were adapted for small-volume samples as described by [47,48]. For the free glycerol measurements, reagents were obtained from Sigma (2.5 µl plasma, 200 µl reagent). Samples were completely randomized and ran in duplicate in a single assay. The inter-assay variations were 8.6% for triglycerides, 7.1% for glycerol, and 5.3% for ALP, and the intra-assay coefficients of variation were 7.2%, 6.9%, and 4.7%, respectively. Actual triglyceride concentration was calculated by subtracting the free glycerol concentration from the total triglyceride concentration.

(c). Isotopic analyses

Isotopic values (δ15N and δ13C values) were measured in whole blood (hereafter, ‘blood’). The isotopic values of the blood samples of adults reflected the prey items assimilated during the courtship period. In the laboratory, blood samples were dried in an oven at 60°C for approximately 24 h and then ground into fine powder. Dried samples were weighed and wrapped in tin capsules. Weights ranged from 700 to 1000 mg. Samples were sent to the Stable Isotope Facility at the University of California, Davis, USA, for δ13C and δ15N analysis. Lipid extraction was not necessary because the C : N mass ratio was less than 3.5 for all blood samples [49]. Isotopic values were obtained for only eight pairs because of the small volume of each blood sample obtained.

(d). Statistical analyses

The strength of the association between mates (triglyceride concentration, δ15N, and δ13C) in BFBO pairs was estimated by the Pearson correlation coefficient [5,50,51] combined with an estimator of mating preference (Crough; [52]). By using the Crough estimator, we avoided ‘false-positive’ results, termed ‘the scale-of-choice effect’. Crough uses a folded Gaussian (normal) distribution function for mating preference to infer the choice (sensu [53]) of the trait in a population. The Crough value was calculated with the CHOICE v. 1.0 program [54]. Additionally, we used the residuals of the regression between triglyceride concentrations in females and males to determine the asymmetry between the members of each pair. This calculation of asymmetry did not include δ15N and δ13C values due to the small sample size. A residual close to 0 corresponds to more symmetrical partners, a value less than 0 indicates that the female had a lower triglyceride concentration than expected based on the male triglyceride concentration, and a value greater than 0 indicates that the female had a higher triglyceride concentration than expected.

To evaluate the effects of assortative mating on reproductive performance, we used a general linear model (GLM), considering total egg volume as a dependent variable and the Sum-Trigls of the pair and asymmetry within the pair as predictor variables. To test whether there were effects of the Sum-Trigls of partners and asymmetry within the pairs on hatching and fledging success, we used a generalized linear model, considering a binomial distribution (successful hatchling/fledgling = 1, no hatchling/fledgling = 0) and a logit link function. Laying order (1–3) or hatching order (A–C) of offspring were included in the model as categorical variables to control for the effect of having a lower probability of hatching in the case of eggs laid later and a lower probability of survival in the case of younger offspring. Sum-Trigls and the residuals from the regression of female–male triglyceride concentrations were included as predictor variables. The Wald test was used to test the statistical significance of each coefficient in the model.

Finally, to evaluate whether there were effects of pair Sum-Trigls and the residuals from the regression of female–male triglyceride concentrations on the ALP concentration (a proxy of growth rate) in the first chick, we used a GLM. By analysing only the first chick, we controlled for potential sibling conflict issues. Age of the offspring at blood sampling (to control for the possible effects of age on ALP concentration), Sum-Trigls, and the residuals from the regression of female–male triglyceride concentrations were included as continuous predictor variables.

Plasma metabolite concentrations depend strongly on food intake, and variation in daily feeding patterns may cause variation in these values [31]. Furthermore, metabolite concentrations can vary according to body size and handling time during sampling [31,55]. As adults and chicks were sampled at different times of the day and had different handling times and body sizes (represented by culmen sizes), we performed a multiple regression analysis to determine whether these variables affected plasma metabolite concentrations; these analyses showed no statistically significant effect (p > 0.05 in all cases). Additionally, for the plasma triglyceride analysis, we included the days before laying, and found no statistically significant effect (p > 0.05). Thus, these variables were excluded from the subsequent analyses. All statistical analyses were performed using STATISTICA 10 [56]. The values reported are the mean ± s.e., and the significance level was set at 0.05.

3. Results

(a). Assortative mating

Triglyceride concentration varied greatly between males and females during the courtship period (females: 12.67 ± 1.74 mmol l−1; males: 1.46 ± 0.13 mmol l−1). There were significant positive relationships between the triglyceride concentrations within a pair (r = 0.83; p < 0.01, figure 1) and the δ15N values within a pair (r = 0.90; p < 0.01, figure 2a); both correlations remained significant when we used the estimator Crough (triglycerides: mean ± s.d. = 0.41 ± 0.25, range [mean Crough of the simulation–mean Crough of the corresponding sample] = 0.27–0.41, p < 0.01; δ15N: mean ± s.d. = 0.58 ± 0.4, range = 0.38–0.58, p < 0.05). For foraging habitat (δ13C), although the correlation coefficient between pair values was high (r = 0.63), the relationship was not significant (p = 0.09, figure 2b); this lack of correlation was corroborated by the Crough value (mean ± s.d. = 0.34 ± 0.26, range = 0.31–0.34, p = 0.35).

Figure 1.

Figure 1.

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Correlation of triglyceride concentration between members of pairs of blue-footed boobies (Sula nebouxii) sampled from the Isla El Rancho colony in Sinaloa, Mexico, during the courtship period.

Figure 2.

Figure 2.

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Correlations of blood δ15N and δ13C values between members of pairs of blue-footed boobies (Sula nebouxii) sampled from the Isla El Rancho colony in Sinaloa, Mexico, during the courtship period.

(b). Breeding performance and offspring fitness

Total egg volume, hatching and fledgling success were related to the Sum-Trigls of the partners (total egg volume: F1,20 = 16.46, p < 0.001, figure 3; hatching success: Wald = 4.74, d.f. = 1, p = 0.03, figure 4a; fledging success: Wald = 7.57, d.f. = 1, p < 0.01, figure 4b) but not to the asymmetry between partners (total egg volume: F1,20 = 1.41, p = 0.24; hatching success: Wald = 0.001, d.f. = 1, p = 0.97; fledging success: Wald = 0.03, d.f. = 1, p = 0.86). Hatching order had a significant effect on fledging success (Wald = 6.49, d.f. = 2, p = 0.04), whereas laying order had no effect on hatching success (Wald = 5.15, d.f. = 2, p = 0.08). Accordingly, a high Sum-Trigls of the partners was associated with an increased total egg volume and higher hatching and fledging success (figures 3 and 4). Moreover, there were progressive reductions in fledging success with increasing hatching order and decreasing Sum-Trigls of the partners (figure 4b).

Figure 3.

Figure 3.

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Relationship between the sum of triglyceride concentrations per pair of blue-footed boobies (Sula nebouxii) during the courtship period and total egg volume (sum of individual egg volumes in the clutch).

Figure 4.

Figure 4.

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Relationship between the sum of triglyceride concentrations per pair of blue-footed boobies (Sula nebouxii) during the courtship period and (a) hatching success (data and estimated probability) and (b) fledging success (data and estimated probability depending on hierarchy). Fitted lines are derived from generalized linear models.

We found a significant positive relationship of Sum-Trigls and within-pair residuals with the ALP concentration of the first chick (Sum-Trigls: F1,12 = 7.77, p = 0.02, figure 5a; asymmetry: F1,12 = 6.35, p = 0.03, figure 5b). Pairs with a higher combined triglyceride concentration and pairs in which the female had a higher triglyceride concentration than expected based on the male triglyceride concentration had offspring with higher ALP values. The age of the offspring had no effect on ALP concentration (F1,12 = 0.85, p = 0.37).

Figure 5.

Figure 5.

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Relationship between the alkaline phosphatase concentration of the first chicks and (a) the sum of triglyceride concentrations per pair of blue-footed boobies (Sula nebouxii) and (b) the asymmetry within each pair (measured as the residuals from a regression of female and male triglyceride concentrations). A value less than 0 indicates that the female had a lower triglyceride concentration than expected based on the male triglyceride concentration, and a value greater than 0 indicates that the female had a higher triglyceride concentration than expected.

4. Discussion

(a). Assortative mating

We found strong assortative mating in a long-lived, socially monogamous seabird as determined by labile traits (body condition and diet). The correlation coefficients found in our study (0.83–0.90) were high relative to the average value (0.28) reported in similar contexts for other animal populations [5]. The high selectivity observed in BFBOs may be a consequence of costly and prolonged reproduction, where both parents exchange information and make decisions accordingly through an honest signalling system based on foot colour. Triglyceride concentration and δ15N values in whole blood, which are both related to body condition and food quality, could be associated with this signalling system.

Assortative mating evaluated based on δ15N values has been reported in some seabird species [12,57], but the benefits of this type of assortative mating remain unclear [12]. One possible benefit is the transfer of information about where to find food resources between mates [12]. However, studies with global positioning system (GPS) devices indicate that within a BFBO pair, the female and male do not use similar foraging areas during contiguous trips, which suggests that such information transfer is not a potential benefit ([58], JA Castillo-Guerrero 2011–2012, unpublished data). In BFBO females, the isotopic composition of whole blood has been found to be associated with variation in plasma triglyceride concentration, with females that feed at a higher trophic level (i.e. consuming a higher quality diet) showing higher triglyceride concentrations and higher reproductive performance than those that feed at lower levels [59]. Relationships between foot colour and the labile traits measured in our study are expected because, as we stated previously, foot colour is an honest signal of current nutritional condition, and diet and triglyceride concentration affect this condition.

The interpretation of correlations between partners regarding labile traits should be performed with caution because they may vary with environmental conditions ([60], and in our data because of the small sample size). This problem can be avoided by measuring the labile trait in multiple years [60], but such data are difficult to obtain and, unfortunately, are not available for BFBOs. Nevertheless, we measured triglyceride concentration during different stages of reproduction (courtship and chick-rearing), and the patterns were consistent throughout the reproductive season (see electronic supplementary material, figure S1); although there was variation in triglyceride concentration between stages, the ‘hierarchical order’ was maintained within each sex. In addition, the correlation between members of a pair was maintained between reproductive stages. Furthermore, between pairs, the relative status of each pair (e.g. higher or lower triglyceride concentration) was maintained, even though the concentrations changed.

Our work was performed during favourable breeding conditions due to high prey availability (with cool oceanographic conditions (negative equatorial sea surface temperature anomalies; Climate Prediction Center http://www.nws.noaa.gov)), and assortative matting was strong. However, in years with low prey availability, fewer individuals or pairs might reach the minimum body condition required to reproduce [61]; thus, the strength of assortative mating may vary among years, increasing selectivity during poor years. In years with low prey availability, in addition to potentially not finding a suitable partner, BFBO individuals might forgo reproduction to prioritize survival and future reproductive success, being long-lived animals.

(b). Breeding performance and offspring fitness

There was a large difference between males and females in triglyceride concentration during the courtship period. We must be cautious when interpreting this difference because an approximately 11 times higher triglyceride concentration in females than in males does not necessarily imply that females have a better body condition and can, therefore, invest more in reproduction. There are several physiological processes that can cause such variation in triglyceride concentration. In females, a high intake of lipids during courtship can help meet the demands of gonadal growth and egg production and can provide a buffer of body reserves for the remainder of the breeding season [62]. Moreover, the plasma concentration of triglycerides increases when they are transported in the form of yolk-targeted very-low-density lipoprotein to growing follicles [63,64]. Rapid follicular growth precedes egg laying and spans a few days to a few weeks depending on the species. Another potential explanation for higher triglyceride concentrations in females than in males is the female-biased consumption of lipid-rich prey [65]; however, based on a comparison of the C and N isotopic profiles, there is no evidence of sex differences in prey consumption [39] (figure 2). Moreover, the triglyceride concentration in female BFBOs decreases abruptly after egg laying and remains at a value similar to that in males during the rest of the breeding season [35]. Therefore, it is more feasible that egg production is the physiological process (as pointed out above) resulting in the disparity in triglyceride concentration during the courtship period. Few studies have evaluated plasma metabolites in seabirds during the breeding period [33–35], but this sex difference in triglyceride levels could be a common pattern among seabirds. Studies in other seabird species during the breeding period are needed to evaluate this possibility.

Given the discrepancy in triglyceride concentrations between sexes, we also explored whether the breeding performance was driven by triglyceride values of only females (see electronic supplementary material, additional analyses S1, and electronic supplementary material table S1) by evaluating the separate effects of males, females, and the sum of triglyceride values per pair. These additional analyses indicated that assortative mating was driving our results, rather than the overweighting of triglyceride values of females.

Because the pair triglyceride concentration correlated strongly with reproductive performance and offspring ALP concentration, it is a reliable pair-quality index. We showed that assortative mating based on labile traits, which is associated with visual signalling of foot colour, has short-term fitness consequences for a long-lived, socially monogamous seabird. For example, high values of the sum of triglyceride concentrations in a pair were related to higher total egg volume and higher hatching and fledging success, i.e. higher fitness (figures 3 and 4). Similar patterns have been previously documented but at the individual scale (individual body condition; [66–69]). The effects of assortative mating on reproductive success and offspring ALP concentration highlight the important role of mate choice in this species. Assortative mating based on traits linked to body condition may provide an adaptive advantage because if both parents are similar, they can invest to a greater or lesser extent in reproduction depending on their collective capacity. For example, if both members of pairs have a poor body condition, then reproductive investment will be limited (either because they have more opportunities to reproduce in the future as long-lived animals or because their body condition limits the amount of reproductive investment they can make). Whereas recent studies examining assortative mating were correlational and did not link this mating pattern to fitness [12,13,70,71], the present research provides insight into the (short-term) reproductive consequences of assortative mating in terms of breeding success (figure 4), advancing our understanding of the repercussions of mate choice in seabirds.

Within a pair, asymmetry in triglyceride concentration did not influence any reproductive parameters, but the ALP concentration of their offspring was related to within-pair female condition. This finding implies that females have a stronger influence on their offspring than do males, contributing more to reproduction, which indicates that such investment depends more on their condition than on that of their partners. In the BFBO, females are larger (5–10%) and heavier (30–32%) than males (reversed sexual size dimorphism), and females can provide two to five times more food to the chicks than males can [72,73]. Thus, when food demands are high, the females take up a higher feeding burden than males. This difference could be due to females having a better physiological buffer than males [74] and larger body size [73], which can imply a greater capacity to carry food to chicks. The effect within the pairs was weaker than the effect of assortative mating (between-pair differences) itself. Asymmetry is, therefore, limited by pair choice, and remaining small differences do not play a dominant role in the BFBO reproductive model. Nevertheless, for females, it seems essential to obtain the best possible male, instead of avoiding asymmetry, to maximize the chances for their offspring. However, if females have a buffer (i.e. a higher triglyceride concentration than expected based on their partner's concentration), they can compensate for reduced partner investment within limits.

Our study suggests that BFBOs benefit from coordinated and bidirectional mate choice (when selecting each other according to foot colour, which is associated with triglyceride concentration and δ15N values); this result provides insight into why mates divorce at a high rate (approx. 50%) [23]. Divorce can occur when the net benefit of matching with a different individual exceeds that of staying with a sub-optimal partner [17,75]. Therefore, the incidence of divorce in a population should be determined (at least in part) by the degree of assortative mating according to quality, as noted by [75].

We suggest that future studies evaluate the long-term pattern of assortative mating within the same individuals under different environmental scenarios, evaluating divorce rates, sabbaticals over the lifespan of the animal, and extra-pair copulations as possible mechanisms to mitigate the effects of pairing with sub-optimal individuals. Finally, our study confirms that the use of labile physiological traits can help identify assortative mating, especially when there are no evident (visible) and measurable traits.

Supplementary Material

Additional analyses S1;Supplementary Table S1 ;Supplementary Figure S1
rspb20192578supp1.pdf (227.1KB, pdf)
Reviewer comments
rspb20192578_review_history.pdf (1.3MB, pdf)

Acknowledgements

We thank M. Guevara, A. Mendoza, M. Leal, M. Arvizú, M. Lerma, F. Quesada, J.P. Ceyca, A. Leal, D. Brito, C. Franco, and N. Albano for their help with the fieldwork and I. Piedad, M. Barradas, and S. Herzka for laboratory support. Finally, we thank the three anonymous reviewers for their helpful comments on an earlier draft of the manuscript.

Ethics

The work met the Mexican legal requirements regarding animal welfare, and fieldwork was supervised and approved by Dirección General de Vida Silvestre, Secretaría de Gestión para la Protección Ambiental (SGPA/DGVS/62712/12).

Data accessibility

The dataset generated and/or analysed during the current study is available in the Dryad Digital Repository: https://dx.doi.org/10.5061/dryad.nzs7h44nb [76].

Authors' contributions

E.G.-M., J.A.C.-G., and G.F. conceived the idea and designed the methodology; E.G.-M. and J.A.C.-G. collected the data; E.G.-M. analysed the data; and E.G.-M. led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for submission for publication.

Competing interests

The authors declare that they have no conflicts of interest.

Funding

This work was supported by Fondo Mexicano para la Conservación de la Naturaleza A.C. (grant no. PIE-2012-A-P-C-IGSI-12-12), CONACYT (grant no. I010/176/2012) and Sonoran Joint Venture. E.G.M. was supported by a postdoctoral fellowship from the National Council of Science and Technology (grant no. 473980).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. González-Medina E, Castillo-Guerrero JA, Masero JA, Fernández G. 2020. Data from: Mate selection based on labile traits affects short-term fitness in a long-lived seabird Dryad Digital Repository. ( 10.5061/dryad.nzs7h44nb) [DOI] [PMC free article] [PubMed]

Supplementary Materials

Additional analyses S1;Supplementary Table S1 ;Supplementary Figure S1
rspb20192578supp1.pdf (227.1KB, pdf)
Reviewer comments
rspb20192578_review_history.pdf (1.3MB, pdf)

Data Availability Statement

The dataset generated and/or analysed during the current study is available in the Dryad Digital Repository: https://dx.doi.org/10.5061/dryad.nzs7h44nb [76].

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

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