Conceived and designed the experiments: RF LG. Performed the experiments: RF. Analyzed the data: RF. Contributed reagents/materials/analysis tools: LG. Wrote the paper: RF LG.
The authors have declared that no competing interests exist.
Demographic parameters such as birth and death rates determine the persistence of populations. Understanding the mechanisms that influence these rates is essential to developing effective management strategies. Alloparental behavior, or the care of non-filial young, has been documented in many species and has been shown to influence offspring survival. However, the role of alloparental behavior in maintaining population viability has not been previously studied. Here, we provide the first evidence for adoption in California sea lions and show that adoption potentially works to maintain a high survival rate of young and may ultimately contribute to population persistence. Alloparental behavior should have a positive effect on the population growth rate when the sum of the effects on fitness for the alloparent and beneficiary is positive.
Alloparental behavior, the care of non-filial young, has been widely documented in mammal and bird species
In California sea lions (
All procedures were approved by the Arizona State University Animal Care and Use Committee (07-918R).
Pups were captured at approximately 4 days to 8 weeks of age in June and July of 2005–2008 at San Jorge and Los Islotes Islands in the Gulf of California (
Study sites included breeding colonies on San Jorge Island (north) and Los Islotes Island (south), in the Gulf of California, Mexico.
DNA was isolated from tissue samples and amplified at 14 microsatellite loci (
Genetic relatedness between female-pup pairs was calculated with the Microsoft Excel Macro ‘
To examine the potential consequences of adoption for population viability, we estimated the discrete rate of annual population growth (λ) based on a Leslie matrix model with fecundity and survival estimates for 19 age classes at Los Islotes Island
We documented mismatches at ≥2 loci for 6 out of 109 sampled female-pup pairs from San Jorge Island, and 9 out of 51 pairs from Los Islotes Island. Additionally, we documented adoption events for two female-pup pairs at San Jorge Island. In both cases, females exhibited distinctive scar patterns, allowing us to track both the female and pup over time. In the first case, the female-pup pair was first identified (and sampled) in August 2007. In October of 2008, the same female was observed nursing the pup tagged in 2007 while simultaneously nursing a new pup from 2008. In the second case, a marked female was observed calling for her pup and receiving no response for three days in June 2008. In July and August of the same year, she was observed nursing a marked pup on multiple occasions (
Female nursing a non-filial pup marked with the haircut ‘A1’. Unique scars on this female, particularly the absence of both hind flippers, allowed researchers to identify her and her pup throughout the field season.
Because there are significant differences in background allele frequencies between San Jorge and Los Islotes Islands
Mean pairwise relatedness (r-values) between filial, non-filial, and randomly generated female-pup pairs on Los Islotes and San Jorge rookeries. Relatedness between non-filial female-pup pairs is no different than expected at random. Error bars represent 1 standard deviation from the mean.
We estimated λ = 1.125 for Los Islotes Island based on vital rates reported in Gerber
Increased pup survival rates result from adoption of orphaned pups and potentially affect the overall population growth rate and long-term population viability. a) Change in population growth rate (λ) resulting from reductions in pup survival in the absence of adoption (solid bars) and reductions in female fecundity as a cost to adopting (hashed bars) for a range of observed adoption rates; b) Projected abundance at Los Islotes in 50 years for a range of underlying rates of population growth under alternative assumptions about adoption reflecting the small changes in λ portrayed in
In this study, we found that adoption occurs in natural populations of California sea lions by combining genotypic and behavioral data from two female-pup pairs. Repeated observations of these individuals confirmed that, although non-filial, each relationship mirrored that of conventional female-pup pairs. A more extensive analysis of genetic maternity suggested that adoptive female-pup pairs accounted for less than 6% of the female-pup pairs on San Jorge Island. This is consistent with studies of other otariids (fur seals and sea lions), including the Steller sea lion
Because most females do not bear identifying marks, incidents where a pup nursed from multiple females or where a female nursed two or more pups on separate occasions would have gone undetected. Thus, it is possible that mismatches do not always represent actual adoption events. Instead mismatches could result from pups stealing milk from unrelated females, or reciprocal nursing (i.e. females willingly nurse each other's pups)
Reciprocal nursing is generally restricted to cases where nearly all females participate
Discussion of the population-level effects of an altruistic trait such as alloparenting frequently centers on the topic of Multilevel Selection Theory which explains the evolution of such traits via their advantage to the group
Under the right circumstances, alloparenting may help maintain population size and persistence. We show that adoption in a California sea lion colony has the potential to influence long-term population growth and that these population-level benefits can be seen even when adoption is infrequent (
We predict that alloparental behavior will have a positive effect on λ when the sum of its effects on lifetime reproductive output for the alloparent and beneficiary is positive. This will occur when alloparental behavior i) provides a neutral or positive effect on the reproductive output of the alloparent or ii) provides a net increase in the reproductive output of the beneficiary that is greater than the net decrease of reproductive output incurred by the alloparent. This assumes that there is no difference between the fitness of offspring produced by the alloparent and offspring produced by the beneficiary. Our results are broadly relevant for all forms of alloparental care and across taxa.
The number of observed alleles and expected heterozygosity (HE) for each locus.
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Special thanks to Misuzu Toyama, whose observations and expertise made this work possible.