Environmental mismatch results in emergence of cooperative behavior in a passerine bird

A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent's nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.NSF [DGE-1143953, DEB-918095, DEB-1350107]12 month embargo; published online: 07 March 2018This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Condition-dependent sexual traits and social dominance in the house finch

Elaboration of costly sexual traits can reduce investment in other aspects of reproduction, such as parental care or intrasexual competition, which may lead to the evolution of alternative mating tactics. In house finches (Carpodacus mexicanus), less elaborately ornamented (dull) males tend to dominate more elaborated (redder) males, but redder males pair earlier and invest more in parental care. This suggests that males may pursue alternative parental or competitive tactics, depending on the elaboration of their sexual trait. Elevation of testosterone, a hormone that is closely associated with condition in male house finches, influences dominance and sexual behaviors but is antagonistic to parental behaviors. We tested the hypothesis that the higher dominance status of dull males reflects an alternative testosterone-dependent mating tactic. First, we experimentally manipulated the testosterone levels of captive males and measured the effect on dominance rank, and second, we measured the association of testosterone elevation and plumage hue in free-living males. We found that, as predicted, testosterone elevation increased dominance rank in captive males. However, in free-living males, testosterone levels were higher in redder males, suggesting that testosterone is dissociated from dominance status under natural circumstances. This may be because the context of social interactions and the higher motivation of dull males to access food resources have a stronger influence on the outcome of dominance interactions than does the physiological effects of testosterone elevation. In turn, the strong positive correlation between testosterone levels and plumage elaboration likely reflects the common condition dependence of these traits. Copyright 2004.condition-dependent; house finch; sexual ornament; testosterone

A condition dependent link between testosterone and disease resistance in the house finch.

Testosterone has recently been proposed as a link between male quality and health and the expression of sexual traits. We investigated the relationship between testosterone and measures of the individual condition and health of males in a natural population of house finches (Carpodacus mexicanus). We also conducted a captive experiment in order to test for the effects of testosterone on resistance to coccidia, which is a common parasite of house finches. Free-living males in better condition had higher testosterone levels and lower corticosterone levels than free-living males in poor condition. In our captive experiment, increased testosterone accelerated the rate of coccidial infection as compared with sham-implanted or gonadectomized males. Although the differences were not significant, free-living males infected with coccidia had lower levels of testosterone and higher levels of corticosterone than males that were not infected. Thus, experimentally elevating testosterone levels in captive males resulted in a higher percentage of infected males, while free-living males with coccidial infection had low testosterone levels. This apparent discrepancy between captive and free-living males in the association of testosterone and disease may be explained by the condition dependence of testosterone. These results suggest that the testosterone-dependent sexual traits reliably indicate male overall condition and health and, thus, females could benefit from assessing potential mates based on these traits

Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range

Environmental mismatch results in emergence of cooperative behavior in a passerine bird

A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent's nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.NSF [DGE-1143953, DEB-918095, DEB-1350107]12 month embargo; published online: 07 March 2018This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

S4_Data_xlsx

Published data (Fig 1A): Excel spreadsheet containing two separate sheets with data from literature: 1) data extracted from the publications and 2) the original references

S3_Data.xlsx

Unpublished data (nine long-term field studies): Data where we combined the information from data S1_Data and S2_Dat

PRISMA_literature summary

The process of literature investigation

S6_Data_xlsx

Models for the unpublished data (Fig 1C): Excel spreadsheet contains 6 separate sheets; each sheet corresponds to a model to estimate the strength of assortative mating

S1_Data.xlsx

Unpublished data (nine long-term field studies): All the pairs that have been identified across the nine studies where both pair members have at least one morphological record, including repeated records from different years. This dataset also includes latitude and longitude of the nest site (Lambert azimuthal equal-area projection, units = meters) and year and, if available, the putative date of the first egg