Elena C. Berg

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.

Reverse sex‐biased philopatry in a cooperative bird: genetic consequences and a social cause

The genetic structure of a group or population of organisms can profoundly influence the potential for inbreeding and, through this, can affect both dispersal strategies and mating systems. We used estimates of genetic relatedness as well as likelihood‐based methods to reconstruct social group composition and examine sex biases in dispersal in a Costa Rican population of white‐throated magpie‐jays (Calocitta formosa, Swainson 1827), one of the few birds suggested to have female‐biased natal philopatry. We found that females within groups were more closely related than males, which is consistent with observational data indicating that males disperse upon maturity, whereas females tend to remain in their natal territories and act as helpers. In addition, males were generally unrelated to one another within groups, suggesting that males do not disperse with or towards relatives. Finally, within social groups, female helpers were less related to male than female breeders, suggesting greater male turnover within groups. This last result indicates that within the natal group, female offspring have more opportunities than males to mate with nonrelatives, which might help to explain the unusual pattern of female‐biased philopatry and male‐biased dispersal in this system. We suggest that the novel approach adopted here is likely to be particularly useful for short‐term studies or those conducted on rare or difficult‐to‐observe species, as it allows one to establish general patterns of philopatry and genetic structure without the need for long‐term monitoring of identifiable individuals.

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.

A TEST OF SEX-RATIO BIASING IN THE WHITE-THROATED MAGPIE-JAY, A COOPERATIVE BREEDER WITH FEMALE HELPERS

Abstract Recent studies suggest that many bird species are able to vary the sex ratio of their young. Among cooperative breeders, in which adult helpers aid the genetic parents in the rearing of young, two models have been invoked to explain this variation. According to the local resource competition hypothesis, parents should bias offspring sex ratios toward the dispersing sex in order to minimize competition for local resources. In contrast, the local resource enhancement (or “production of helpers”) hypothesis states that parents should overproduce the nondispersing sex if the presence of relatives enhances reproductive success. I examined these models in a Costa Rican population of White-throated Magpie-Jays (Calocitta formosa), a cooperatively breeding corvid with female helpers. Using DNA microsatellite analysis, I sexed 135 offspring from 38 broods and 14 groups over 3 years. I tested for variation in offspring sex ratio at the population level and as a function of social group, helper number, breeding female, and season. Unlike studies of the Seychelles Warbler (Acrocephalus sechellensis), one of the few other avian species with primarily female helpers, I found no evidence for systematic sex-ratio bias supporting either hypothesis. This suggests that female-biased helping is not a sufficient condition for the evolution of offspring sex-ratio biasing. Estudio del Sesgo en el Cociente de Sexos en Calocitta formosa, una Reproductora Cooperativa con Ayudantes Hembras Resumen. Estudios recientes sugieren que muchas especies de aves pueden hacer variar el cociente de sexos de sus crías. Se han utilizado dos modelos teóricos para explicar esta variación en las aves que se reproducen en forma cooperativa, en las cuales los adultos ayudan a los padres genéticos con el cuidado de sus crías. Según la hipótesis de competencia por recursos locales, los padres deben sesgar el cociente de sexos de su prole en favor del sexo que se dispersa con el fin de minimizar la competencia por los recursos locales. Por el contrario, según la hipótesis de incremento de recursos locales (o “producción de ayudantes”), los padres deben sobreproducir el sexo que no se dispersa si la presencia de parientes favorece el éxito reproductivo. Yo estudié estos modelos en una población costarricense de urracas (Calocitta formosa), un córvido de reproducción cooperativa con ayudantes hembras. Utilicé análisis de ADN microsatelital para averiguar el sexo de 135 crías provenientes de 38 nidadas y 14 grupos a lo largo de un período de tres años. Documenté las variaciones en el cociente de sexos de las crías a nivel poblacional y como función del grupo social, la cantidad de ayudantes, la hembra reproductiva y la estación del año. A diferencia de lo encontrado para el caso de Acrocephalus sechellensis, una de las pocas especies de aves con ayudantes principalmente hembras, no encontré indicios de sesgo sistemático en el cociente de sexos que avalara ninguna de las dos hipótesis. Esto sugiere que la ayuda por parte de las hembras no constituye una condición que determine la evolución de un sesgo en el cociente de sexos de las crías.

Evolution of differential maternal age effects on male and female offspring development and longevity

Summary 1. Maternal age effects on life-history traits, including longevity, are widespread and can be seen as a manifestation of ageing. However, little is known about how maternal life span may influence the maternal age effect. At a given chronological age, a long-lived parent may be at a younger biological age than a short-lived parent and thus has a less severe parental age effect. However, earlier work using experimentally evolved short- and long-lived lines did not support this hypothesis. 2. We scored developmental time and longevity of 14 995 individual seed beetles, Callosobruchus maculatus derived from replicate short-lived and long-lived lines created via artificial selection on male life span. 3. Offspring from older mothers had shorter life span, which is consistent with most of the literature. 4. We found support for the hypothesis that detrimental maternal age effects evolve to be weaker under selection for long life span. However, this finding was only apparent in males, suggesting that maternal age affects male and female offspring differently. 5. These results suggest that sex-dependent parental age effects should be incorporated in the studies of longevity and ageing evolution and that selection on one sex can cause evolution of parental age effects in the other sex.

SMALL-SCALE DIVERGENCE IN EGG COLOR ALONG AN ELEVATION GRADIENT IN THE MEXICAN JAY (APHELOCOMA ULTRAMARINA): A CONDITION-DEPENDENT RESPONSE?

ABSTRACT. The functional significance of bird egg color and patterning is a continuing subject of interest and debate. Extreme polymorphism in eggshell appearance is often thought to be maintained by frequency-dependent selection operating within populations. However, variation could also be explained by small-scale differentiation combined with limited migration. Here, we report the existence of extreme variation in egg color in a population of Mexican Jays (Aphelocoma ultramarina) inhabiting a steep elevation and habitat gradient within a single mountain range, the Sierra del Carmen of Coahuila, Mexico. We quantified egg color of 143 eggs from 54 nests throughout the mountain range, using digital photos. Color was also quantified for a subset of these eggs, using a spectrometer. Results from both methods support the conclusion that egg color has diverged at a remarkably small spatial scale of 3–15 km. Photo color quantification indicated that eggs at high elevation were greener than those at low elevation. Spectrometer results supported this conclusion, with more-pigmented (i.e., less reflectant) eggs occurring at high elevation. Unlike in other species, differences in condition do not seem to drive these divergence patterns in egg color. Further study is needed to determine to what extent differences result from heritable genetic change attributable to divergent selection pressures or from an environmentally induced phenotypic response.

New phylogenetic information suggests both an increase and at least one loss of cooperative breeding during the evolutionary history of Aphelocoma jays

Efforts to identify ecological and life history factors associated with cooperative breeding have been largely unsuccessful, and interest is growing in the role of phylogenetic history in determining the distribution of this social system among lineages. In birds, cooperative breeding is distributed non-randomly among lineages, suggesting that phylogenetic inertia may play an important role in determining its distribution. The bird genus Aphelocoma has been particularly well studied because, although it is a relatively small genus, it shows broad among-lineage variation in level of cooperation. Previous analyses described an unusual unidirectional pattern of evolutionary loss of cooperation in Aphelocoma. Here, historical reconstructions based on new phylogenetic data suggest that evolutionary changes in cooperation have been bidirectional, with at least one gain and at least one loss over relatively recent timescales. This result emphasizes that, although history plays an important role in determining the incidence of cooperative breeding, cooperative behavior can switch relatively quickly in evolutionary time and may be influenced by the ecological context within which particular populations are distributed.

What determines the timing and duration of the nesting season for a tropical dry forest bird, the White-throated Magpie-Jay (Calocitta formosa)?

ABSTRACT The factors affecting the timing of nesting in tropical birds remain poorly understood. We investigated the phenology of White-throated Magpie-Jay (Calocitta formosa) nesting in the dry forest of northwest Costa Rica, a region characterized by a severe 5-month dry season followed by a very rainy wet season. We examined whether nesting was associated with climate, diet, risk of parasite infection to nestlings, risk of nest predation, and opportunity to re-nest. Groups of White-throated Magpie-Jays nested repeatedly, initiating nests over a 7-month period that spanned the transition from the dry to early wet season. The diet of adults and the composition of food fed to broods varied seasonally in parallel with changes in vegetation condition and climate associated with the transition from dry to wet season. Fledgling transition to nutritional independence occurred exclusively in the wet season when caterpillars and other arthropods were a large component of the diet. The timing of groups’ last nests was associated with an increase in nestling infections by Philornis botflies. We argue that progress at understanding tropical birds’ nesting seasons will be made by looking beyond diet and climate at the time of nesting, to additional factors such as the conditions during the post-fledging period of offspring development, temporal patterns of risk of parasite and pathogen infection to nestlings, and temporal patterns of nest or fledgling predation risk.