Luke J. Eberhart-Phillips

Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals

Significance Understanding olfactory communication in natural vertebrate populations requires knowledge of how genes and the environment influence highly complex individual chemical fingerprints. To understand how relevant information is chemically encoded and may feed into mother–offspring recognition, we therefore generated chemical and genetic data for Antarctic fur seal mother–pup pairs. We show that pups are chemically highly similar to their mothers, reflecting a combination of genetic and environmental influences. We also reveal associations between chemical fingerprints and both genetic quality and relatedness, the former correlating positively with substance diversity and the latter encoded mainly by a small subset of substances. Dissecting apart chemical fingerprints to reveal subsets of potential biological relevance has broad implications for understanding vertebrate chemical communication. Chemical communication underpins virtually all aspects of vertebrate social life, yet remains poorly understood because of its highly complex mechanistic basis. We therefore used chemical fingerprinting of skin swabs and genetic analysis to explore the chemical cues that may underlie mother–offspring recognition in colonially breeding Antarctic fur seals. By sampling mother–offspring pairs from two different colonies, using a variety of statistical approaches and genotyping a large panel of microsatellite loci, we show that colony membership, mother–offspring similarity, heterozygosity, and genetic relatedness are all chemically encoded. Moreover, chemical similarity between mothers and offspring reflects a combination of genetic and environmental influences, the former partly encoded by substances resembling known pheromones. Our findings reveal the diversity of information contained within chemical fingerprints and have implications for understanding mother–offspring communication, kin recognition, and mate choice.

Conservation challenges of a sink: the viability of an isolated population of the Snowy Plover

Source-sink dynamics are easily overlooked when formulating recovery objectives for threatened species. This could lead to unrealistic criteria imposed on sink populations, which in turn might restrict an entire metapopulation from being delisted. Therefore, an understanding of the viability of subpopulations within the context of a metapopulation is needed to develop appropriate recovery objectives. Consequently, we used 11 years of mark-recapture, productivity, and movement data to analyse the viability of a small, geographically isolated population of the Snowy Plover Charadrius nivosus, a shorebird listed as threatened under the U.S. Endangered Species Act. Simulations confirmed that the focal population in northern California is a sink that relies upon immigrants from neighbouring populations. Furthermore, these source populations will increase within the next 50 years and are likely to achieve the delisting requirements. However, the northern California population is unlikely to reach the delisting criteria given the current vital rate estimations. Management scenarios demonstrated that lethal predator removal and reducing human disturbance facilitate population recovery and may partially alleviate the reliance upon immigration. However, the use of nest exclosures reduced population growth because they are known to compromise adult survival. These results highlight the importance of maintaining viable source populations and re-evaluating the recovery objectives of metapopulations with active sinks.

Contrasting genetic diversity and population structure among three sympatric Madagascan shorebirds: parallels with rarity, endemism, and dispersal

Understanding the relative contributions of intrinsic and extrinsic factors to population structure and genetic diversity is a central goal of conservation and evolutionary genetics. One way to achieve this is through comparative population genetic analysis of sympatric sister taxa, which allows evaluation of intrinsic factors such as population demography and life history while controlling for phylogenetic relatedness and geography. We used ten conserved microsatellites to explore the population structure and genetic diversity of three sympatric and closely related plover species in southwestern Madagascar: Kittlitzs plover (Charadrius pecuarius), white-fronted plover (C. marginatus), and Madagascar plover (C. thoracicus). Bayesian clustering revealed strong population structure in the rare and endemic Madagascar plover, intermediate population structure in the white-fronted plover, and no detectable population structure in the geographically widespread Kittlitzs plover. In contrast, allelic richness and heterozygosity were highest for the Kittlitzs plover, intermediate for the white-fronted plover and lowest for the Madagascar plover. No evidence was found in support of the “watershed mechanism” proposed to facilitate vicariant divergence of Madagascan lemurs and reptiles, which we attribute to the vagility of birds. However, we found a significant pattern of genetic isolation by distance among populations of the Madagascar plover, but not for the other two species. These findings suggest that interspecific variation in rarity, endemism, and dispersal propensity may influence genetic structure and diversity, even in highly vagile species.

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

Significance Sex biases are widespread in nature and represent a fundamental component of sexual selection and population biology—but at which point in life history do these biases emerge? We report a detailed individual-based demographic analysis of an intensively studied wild bird population to evaluate origins of sex biases and their consequences on mating strategies and population dynamics. We document a strongly male-biased adult sex ratio, which is consistent with behavioral observations of female-biased polygamy. Notably, sex-biased juvenile rather than adult survival contributed most to the adult sex ratio. Sex biases also strongly influenced population viability, which was significantly overestimated when sex ratio and mating system were ignored. Our study, therefore, has implications for both sexual selection theory and biodiversity conservation. 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.

Population structure and historical demography of South American sea lions provide insights into the catastrophic decline of a marine mammal population

Understanding the causes of population decline is crucial for conservation management. We therefore used genetic analysis both to provide baseline data on population structure and to evaluate hypotheses for the catastrophic decline of the South American sea lion (Otaria flavescens) at the Falkland Islands (Malvinas) in the South Atlantic. We genotyped 259 animals from 23 colonies across the Falklands at 281 bp of the mitochondrial hypervariable region and 22 microsatellites. A weak signature of population structure was detected, genetic diversity was moderately high in comparison with other pinniped species, and no evidence was found for the decline being associated with a strong demographic bottleneck. By combining our mitochondrial data with published sequences from Argentina, Brazil, Chile and Peru, we also uncovered strong maternally directed population structure across the geographical range of the species. In particular, very few shared haplotypes were found between the Falklands and South America, and this was reflected in correspondingly low migration rate estimates. These findings do not support the prominent hypothesis that the decline was caused by migration to Argentina, where large-scale commercial harvesting operations claimed over half a million animals. Thus, our study not only provides baseline data for conservation management but also reveals the potential for genetic studies to shed light upon long-standing questions pertaining to the history and fate of natural populations.

Spatial synchrony of a threatened shorebird: Regional roles of climate, dispersal and management

Summary Correlated climate patterns, dispersal, and similar management practices may synchronise dynamics of populations in close proximity, which tends to reduce metapopulation persistence. However, synchronising and desynchronising mechanisms can act at multiple spatial scales, which means that for wide-ranging species, patterns of spatial synchrony and their causes might vary across the species’ range. We examined the relationships of spatial autocorrelation in winter climate, dispersal distance and predator management to the spatio-temporal dynamics of the Western Snowy Plover Charadrius nivosus nivosus , a threatened shorebird that breeds along the Pacific coast of the United States. We investigated how signals and drivers of plover population growth dynamics vary among populations occupying northern, central, and southern regions of the species’ U.S. range. Across the metapopulation and specifically the core of the species’ range in the south, we found that plover populations within 132 km of each other exhibited detectable levels of synchrony, which fell within published estimates of dispersal distance. Furthermore, similar predator management among sites increased the degree to which nearby populations were synchronised. There was, however, no evidence of spatial synchrony in populations of the northern and central regions. Regional differences in synchrony were associated with different population drivers and structure; prolonged cold periods had the strongest influence on the growth of northern populations while predator management had the strongest influence on southern populations. Northern populations were also smaller than the south, which likely reduced our ability to detect spatial synchrony because of increased demographic stochasticity. Neither climatic nor management variables had a detectable influence on central populations. Although the primary objective of threatened and endangered species management is to increase populations to viable levels, we recommend that conservation biologists and land managers acknowledge region-specific processes when considering the long-term persistence of wide-ranging species and coordinate inter-agency efforts to manage neighbouring populations effectively .

Adult sex ratio bias in snowy plovers is driven by sex-specific early survival: implications for mating systems and population growth

Adult sex ratio (ASR) is a central concept in population biology and a key factor in sexual selection, yet 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 is primarily driven by sex-specific survival of juveniles, rather than adults or dependent offspring. This 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 is most sensitive to perturbations in survival of the limiting sex. Overall, our study suggests that sex-biased early survival may contribute towards mating system evolution and population persistence, with implications for both sexual selection theory and biodiversity conservation. SIGNIFICANCE STATEMENT Sex biases are widespread in nature and represent a fundamental component of sexual selection and population biology—but at which point in life history do these biases emerge? Here we report a detailed individual-based demographic analysis of an intensively studied wild bird population to evaluate the origins of sex biases and their consequences on mating strategies and population dynamics. We document a strongly male-biased adult sex ratio, which is consistent with behavioral observations of female-biased polygamy. Notably, sex-biased juvenile, rather than adult survival, contributed most to the adult sex ratio. Sex-biases also strongly influenced population viability, which was significantly overestimated when sex ratio and mating system were ignored. Our study therefore has implications for both sexual selection theory and biodiversity conservation.

Extremely low Plasmodium prevalence in wild plovers and coursers from Cape Verde and Madagascar

BackgroundRelatively little is known about the prevalence of blood parasites in shorebirds, especially those breeding in the tropics. The prevalence of blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon was assessed in blood samples from Kentish plovers and cream-coloured coursers in Cape Verde, and samples of Kittlitz’s plovers, Madagascar plovers and white-fronted plovers in Madagascar.ResultsOnly two of these samples were positive for Plasmodium: a Kittlitz’s plover was infected by a generalist lineage of Plasmodium that has already been reported in Europe and Africa, while in a white-fronted plover direct sequencing revealed a previously un-described Plasmodium lineage.ConclusionPotential explanations for the low prevalence of blood parasites include the scarcity of vectors in habitats used by these bird species and their resistance to parasitic infections.

Apparent Survival of Snowy Plovers (Charadrius nivosus) Varies with Reproductive Effort and Year and between Sexes

Abstract. Life history theory predicts a tradeoff between reproductive effort and survival, which suggests that some management practices aimed at increasing productivity may compromise population growth. We analyzed a 10-year data set of 225 individually marked Snowy Plovers (Charadrius nivosus), a threatened shorebird, to determine whether individual reproductive effort was correlated with low apparent survival. Most adults resided in the population an average of 2 years (range: 1–10 years), during which females laid 3–60 eggs, and both males and females invested considerable time in incubation and brooding. Apparent survival varied annually and was higher for males than for females. Contrary to theory, we found no evidence that increased reproductive effort, either current or cumulative, compromised survival. Instead, apparent survival was correlated positively with incubation time, which may be related to either high-quality individuals having high reproductive rates and high survival or permanent emigration of failed breeders (who incubated for shorter intervals). Although our results suggest that some predator management practices (e.g., nest exclosures) aimed at increasing productivity will not compromise survival in a subsequent year, we caution that these same practices may have serious negative consequences for population growth if (1) reproductive effort does not translate into higher per capita fledging success and (2) direct mortality of adults results from the practice.

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.Biases in adult sex ratio (ASR) are common, yet their causes and consequences are not well understood. Here, the authors analyse data from >6000 individuals of five shorebird species, showing that sex differences in juvenile survival drive ASR variation and biased ASR is associated with uniparental care.