Egg size variation in the context of polyandry: a case study using long-term field data from snowy plovers.

Gamete size variation between the sexes is central to the concept of sex roles, however, to what extent gamete size variation within the sexes relates to sex role variation remains unclear. Comparative and theoretical studies suggest that, when clutch size is invariable, polyandry is linked to a reduction of egg size, while increased female-female competition for mates favors early breeding when females cannot monopolize multiple males. To understand whether and how breeding phenology, egg size, and mating behavior are related at the individual level, we studied the reproductive histories of 424 snowy plover females observed in the wild over a 15-year period. Egg size, but not polyandry, were highly repeatable for individual females. Consistent with theoretical predictions, we found that polyandrous females were the earliest breeders and that early clutches contained smaller eggs than clutches initiated later. Neither egg size nor mating behavior showed clear signs of an age-related deterioration, on the contrary, prior experience acquired either through age or local recruitment enabled females to nest early. Taken together, these results suggest that gamete size variation is not linked to mating behavior at the individual level, and, consequently, the adaptive potential of such variation appears to be limited.

Allelic diversity and patterns of selection at the major histocompatibility complex class I and II loci in a threatened shorebird, the Snowy Plover (Charadrius nivosus).

BACKGROUND: Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classical MHC genes show high polymorphism and are under strong balancing selection, as their products trigger the adaptive immune response in vertebrates. Here, we assess the allelic diversity and patterns of selection for MHC class I and class II loci in a threatened shorebird with highly flexible mating and parental care behaviour, the Snowy Plover (Charadrius nivosus) across its broad geographic range. RESULTS: We determined the allelic and nucleotide diversity for MHC class I and class II genes using samples of 250 individuals from eight breeding population of Snowy Plovers. We found 40 alleles at MHC class I and six alleles at MHC class II, with individuals carrying two to seven different alleles (mean 3.70) at MHC class I and up to two alleles (mean 1.45) at MHC class II. Diversity was higher in the peptide-binding region, which suggests balancing selection. The MHC class I locus showed stronger signatures of both positive and negative selection than the MHC class II locus. Most alleles were present in more than one population. If present, private alleles generally occurred at very low frequencies in each population, except for the private alleles of MHC class I in one island population (Puerto Rico, lineage tenuirostris). CONCLUSION: Snowy Plovers exhibited an intermediate level of diversity at the MHC, similar to that reported in other Charadriiformes. The differences found in the patterns of selection between the class I and II loci are consistent with the hypothesis that different mechanisms shape the sequence evolution of MHC class I and class II genes. The rarity of private alleles across populations is consistent with high natal and breeding dispersal and the low genetic structure previously observed at neutral genetic markers in this species.

Successful breeding predicts divorce in plovers.

When individuals breed more than once, parents are faced with the choice of whether to re-mate with their old partner or divorce and select a new mate. Evolutionary theory predicts that, following successful reproduction with a given partner, that partner should be retained for future reproduction. However, recent work in a polygamous bird, has instead indicated that successful parents divorced more often than failed breeders (Halimubieke et al. in Ecol Evol 9:10734-10745, 2019), because one parent can benefit by mating with a new partner and reproducing shortly after divorce. Here we investigate whether successful breeding predicts divorce using data from 14 well-monitored populations of plovers (Charadrius spp.). We show that successful nesting leads to divorce, whereas nest failure leads to retention of the mate for follow-up breeding. Plovers that divorced their partners and simultaneously deserted their broods produced more offspring within a season than parents that retained their mate. Our work provides a counterpoint to theoretical expectations that divorce is triggered by low reproductive success, and supports adaptive explanations of divorce as a strategy to improve individual reproductive success. In addition, we show that temperature may modulate these costs and benefits, and contribute to dynamic variation in patterns of divorce across plover breeding systems.

CeutaOPEN, individual-based field observations of breeding snowy plovers Charadrius nivosus.

Shorebirds (part of the order Charadriiformes) have a global distribution and exhibit remarkable variation in ecological and behavioural traits that are pertinent to many core questions in the fields of evolutionary ecology and conservation biology. Shorebirds are also relatively convenient to study in the wild as they are ground nesting and often occupy open habitats that are tractable to monitor. Here we present a database documenting the reproductive ecology of 1,647 individually marked snowy plovers (Charadrius nivosus) monitored between 2006 and 2016 at Bahía de Ceuta (23°54N, 106°57W) - an important breeding site in north-western Mexico. The database encompasses various morphological, behavioural, and fitness-related traits of males and females along with spatial and temporal population dynamics. This open resource will serve as an important data repository for addressing overarching questions in avian ecology and wetland conservation during an era of big data and global collaborative science.

Mate fidelity in a polygamous shorebird, the snowy plover (Charadrius nivosus).

Social monogamy has evolved multiple times and is particularly common in birds. However, it is not well understood why some species live in long-lasting monogamous partnerships while others change mates between breeding attempts. Here, we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover (Charadrius nivosus), a species in which both males and females may have several breeding attempts within a breeding season with the same or different mates. Using 6 years of data from a well-monitored population in Bahía de Ceuta, Mexico, we investigated predictors and fitness implications of mate fidelity both within and between years. We show that in order to maximize reproductive success within a season, individuals divorce after successful nesting and re-mate with the same partner after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher reproductive success than individuals that retain their mate. We also show that different mating decisions between sexes predict different breeding dispersal patterns. Taken together, our findings imply that divorce is an adaptive strategy to improve reproductive success in a stochastic environment. Understanding mate fidelity is important for the evolution of monogamy and polygamy, and these mating behaviors have implications for reproductive success and population productivity.

Nest initiation and flooding in response to season and semi-lunar spring tides in a ground-nesting shorebird.

BACKGROUND: Marine and intertidal organisms face the rhythmic environmental changes induced by tides. The large amplitude of spring tides that occur around full and new moon may threaten nests of ground-nesting birds. These birds face a trade-off between ensuring nest safety from tidal flooding and nesting near the waterline to provide their newly hatched offspring with suitable foraging opportunities. The semi-lunar periodicity of spring tides may enable birds to schedule nest initiation adaptively, for example, by initiating nests around tidal peaks when the water line reaches the farthest into the intertidal habitat. We examined the impact of semi-lunar tidal changes on the phenology of nest flooding and nest initiation in Snowy Plovers (Charadrius nivosus) breeding at Bahía de Ceuta, a coastal wetland in Northwest Mexico. RESULTS: Using nest initiations and fates of 752 nests monitored over ten years we found that the laying season coincides with the lowest spring tides of the year and only 6% of all nests were flooded by tides. Tidal nest flooding varied substantially over time. First, flooding was the primary cause of nest failures in two of the ten seasons indicating high between-season stochasticity. Second, nests were flooded almost exclusively during the second half of the laying season. Third, nest flooding was associated with the semi-lunar spring tide cycle as nests initiated around spring tide had a lower risk of being flooded than nests initiated at other times. Following the spring tide rhythm, plovers appeared to adapt to this risk of flooding with nest initiation rates highest around spring tides and lowest around neap tides. CONCLUSIONS: Snowy Plovers appear generally well adapted to the risk of nest flooding by spring tides. Our results are in line with other studies showing that intertidal organisms have evolved adaptive responses to predictable rhythmic tidal changes but these adaptations do not prevent occasional catastrophic losses caused by stochastic events.

Demographic causes of adult sex ratio variation and their consequences for parental cooperation.

The adult sex ratio (ASR) is a fundamental concept in population biology, sexual selection, and social evolution. However, it remains unclear which demographic processes generate ASR variation and how biases in ASR in turn affect social behaviour. Here, we evaluate the demographic mechanisms shaping ASR and their potential consequences for parental cooperation using detailed survival, fecundity, and behavioural data on 6119 individuals from six wild shorebird populations exhibiting flexible parental strategies. We show that these closely related populations express strikingly different ASRs, despite having similar ecologies and life histories, and that ASR variation is largely driven by sex differences in the apparent survival of juveniles. Furthermore, families in populations with biased ASRs were predominantly tended by a single parent, suggesting that parental cooperation breaks down with unbalanced sex ratios. Taken together, our results indicate that sex biases emerging during early life have profound consequences for social behaviour.

Sex-specific early survival drives adult sex ratio bias in snowy plovers and impacts mating system and population growth.

Adult sex ratio (ASR) is a central concept in population biology and a key factor in sexual selection, but why do most demographic models ignore sex biases? Vital rates often vary between the sexes and across life history, but their relative contributions to ASR variation remain poorly understood-an essential step to evaluate sex ratio theories in the wild and inform conservation. Here, we combine structured two-sex population models with individual-based mark-recapture data from an intensively monitored polygamous population of snowy plovers. We show that a strongly male-biased ASR (0.63) is primarily driven by sex-specific survival of juveniles rather than adults or dependent offspring. This finding provides empirical support for theories of unbiased sex allocation when sex differences in survival arise after the period of parental investment. Importantly, a conventional model ignoring sex biases significantly overestimated population viability. We suggest that sex-specific population models are essential to understand the population dynamics of sexual organisms: reproduction and population growth are most sensitive to perturbations in survival of the limiting sex. Overall, our study suggests that sex-biased early survival may contribute toward mating system evolution and population persistence, with implications for both sexual selection theory and biodiversity conservation.

Camouflage and Clutch Survival in Plovers and Terns.

Animals achieve camouflage through a variety of mechanisms, of which background matching and disruptive coloration are likely the most common. Although many studies have investigated camouflage mechanisms using artificial stimuli and in lab experiments, less work has addressed camouflage in the wild. Here we examine egg camouflage in clutches laid by ground-nesting Snowy Plovers Charadrius nivosus and Least Terns Sternula antillarum breeding in mixed aggregations at Bahía de Ceuta, Sinaloa, Mexico. We obtained digital images of clutches laid by both species. We then calibrated the images and used custom computer software and edge detection algorithms to quantify measures related to three potential camouflage mechanisms: pattern complexity matching, disruptive effects and background color matching. Based on our image analyses, Snowy Plover clutches, in general, appeared to be more camouflaged than Least Tern clutches. Snowy Plover clutches also survived better than Least Tern clutches. Unexpectedly, variation in clutch survival was not explained by any measure of egg camouflage in either species. We conclude that measures of egg camouflage are poor predictors of clutch survival in this population. The behavior of the incubating parents may also affect clutch predation. Determining the significance of egg camouflage requires further testing using visual models and behavioral experiments.