Received Nov 1; Accepted Dec This article has been cited by other articles in PMC. Abstract Among avian cooperative breeders, help in raising offspring is usually provided by males or by both sexes. Sex bias in helping should evolve in response to sex-specific ecological constraints on independent reproduction, with mate shortage for males and breeding vacancy shortage for each sex. Given that male-biased adult sex ratios are prevalent among birds, we predict that male-only helping mainly occurs in temperate species where fast population turnovers deriving from low adult annual survival allow all adult females to hold breeding vacancies, whereas some males overflow as helpers, and both-sex helping in tropical species where saturated habitats prevent not only males, but also females from breeding themselves.
As expected, we found that across species, adult survival increased towards tropical zones and warmer climates, and higher adult survival tended to be associated with both-sex helping. Furthermore, sex bias in helping was predicted by latitude and ambient temperature. Our findings of demographic response of species to climate as a potential determinant of bias in helper sex uncover how ecological constraints operate to limit independent reproduction in sex-specific ways. An interesting phenomenon in association with this social system is sex-specific helping, by males only in some species or by both sexes in others, with female-only helping being very rare [ 2 ].
Interspecific variation in sex bias of helpers also exists among eusocial species, with the cause being attributed to ecological factors as well as haplodiploidy [ 3 ]. However, this question has never formally been addressed in birds [ 4 ], which have cooperative breeding systems different from those found in eusocial taxa.
Therefore, a key step towards understanding interspecific variation in sex-biased helping is to identify which and how ecological constraints act in a sex-specific way. Known constraints may typically be classified into two distinct categories: Obviously, the former must act on males only, and the latter on both sexes, because a breeding vacancy is necessary for successful reproduction in each sex. The fact that male-biased adult sex ratios are most widespread in birds, including cooperative breeders [ 8 , 9 ], inspired us to suggest the following logic for how either constraint may operate.
If species have lower adult survival rates in temperate than tropical zones [ 10 ], population turnover will increase at higher latitudes [ 11 ], given that no latitudinal gradient in annual production of offspring is evident [ 12 ].
As a consequence, breeding vacancies will be readily available for temperate species but limited for tropical species.
By contrast, both-sex helping should occur in species inhabiting the tropics, where slow breeding vacancy turnover would limit reproductive opportunities for both adult males and females. Using a dataset consisting of phylogenetically diverse cooperatively breeding birds, we tested the predictions that i there is a latitudinal decrease in adult annual survival rate across species, ii species with male-only helping are more likely to be associated with a lower adult annual survival rate and species with both-sex helping with a higher adult annual survival rate, and iii the probability of male-only helping increases when species live further away from the equator.
As climates vary systemically across latitudinal gradients, we also investigated interspecific variation in adult survivorship and helping sex in relation to several climate variables to explore the potential climatic mechanism underlying the patterns described here.
Material and methods a Data collection A literature search was conducted to determine adult annual survival rate and sex bias in helping for cooperatively breeding bird species electronic supplementary material, table S1. Since sex-specific data on survival rate were unavailable for many species, we used the average of both sexes for some species where the data were provided. Sex bias in helping was classified as two levels, male-only or both-sex helping, given that few species have female-only helpers.
Species in which all helpers are juveniles dusky moorhens Gallinula tenebrosa or failed breeders long-tailed tits Aegithalos caudatus, silver-throated tits A. Of the species constituting our sample of species, four 2. Our final dataset contained species, including 88 species with information on adult survival rates. We extracted six climate parameters at the sites where social organization of the species in the dataset were studied. These included annual mean temperature, intrayear temperature variation, interyear temperature variation, annual total precipitation, intrayear precipitation variation and interyear precipitation variation from the environmental geographic information system GIS layers see electronic supplementary material, methods.
Ten randomly selected phylogenetic trees from [ 16 ] were used to control for phylogenetic uncertainty. The raw data were z-transformed to allow a comparison of effect sizes among different predictors. When investigating whether latitude or climate affects adult annual survival rate, we included body mass as a covariate, because larger species usually survive better [ 17 ].
In the analyses with more than one predictor variable, we used a stepwise forward regression method to find out the significant predictors for details see electronic supplementary material, methods. The analyses further showed that annual mean temperature and annual total precipitation significantly predicted interspecific variation in adult survivorship, which increased as ambient temperatures and precipitation increased.
Standardized regression coefficients suggested that the effect of latitude on survival rate was similar to that of each of the two climate variables. Four other climate variables were non-significant predictors of adult annual survival rate.