Sara Calhim

Maintenance of sperm variation in a highly promiscuous wild bird

Postcopulatory sexual selection is an important force in the evolution of reproductive traits, including sperm morphology. In birds, sperm morphology is known to be highly heritable and largely condition-independent. Theory predicts, and recent comparative work corroborates, that strong selection in such traits reduces intraspecific phenotypic variation. Here we show that some variation can be maintained despite extreme promiscuity, as a result of opposing, copulation-role-specific selection forces. After controlling for known correlates of siring success in the superb fairy-wren (Malurus cyaneus), we found that (a) lifetime extra-pair paternity success was associated with sperm with a shorter flagellum and relatively large head, and (b) males whose sperm had a longer flagellum and a relatively smaller head achieved higher within-pair paternity. In this species extrapair copulations occur in the same morning, but preceding, pair copulations during a females fertile period, suggesting that shorter and relatively larger-headed sperm are most successful in securing storage (defense), whereas the opposite phenotype might be better at outcompeting stored sperm (offense). Furthermore, since cuckolding ability is a major contributor to differential male reproductive output, stronger selection on defense sperm competition traits might explain the short sperm of malurids relative to other promiscuous passerines.

Selection on sperm morphology under relaxed sperm competition in a wild passerine bird

Theories regarding the role of sexual selection on the evolution of sperm traits are based on an association between pre-copulatory (e.g. female preference) and post-copulatory (e.g. ejaculate quality) male reproductive traits. In tests of these hypotheses, sperm morphology has rarely been used, despite its high heritability and intra-individual consistency. We found evidence of selection for longer sperm through positive phenotypic associations between sperm size and the two major female preference traits in the pied flycatcher, Ficedula hypoleuca. Our results support the sexually selected sperm hypothesis in a species under low sperm competition and demonstrate that natural and pre-copulatory sexual selection forces should not be overlooked in studies of intraspecific sperm morphology evolution.

Heterospecific female mimicry in Ficedula flycatchers.

Mimicry is a widespread phenomenon. Vertebrate visual mimicry often operates in an intraspecific sexual context, with some males resembling conspecific females. Pied flycatcher (Ficedula hypoleuca) dorsal plumage varies from the ancestral black to female‐like brown. Experimental studies have shown that conspecific and heterospecific (collared flycatcher, F. albicollis) individuals of both sexes respond, at least initially, to brown individuals as if they were female. We quantified the perceptual and biochemical differences between brown feathers and found that brown pied flycatcher males are indistinguishable from heterospecific, but not from conspecific, females in both aspects. To our knowledge, this is the first evidence of a visual mimetic signalling system in a sexual context where the model is heterospecific to the mimic. By only mimicking heterospecific females, brown pied flycatcher males can establish territories next to the more dominant collared flycatcher in sympatry, suffer less aggression by darker conspecifics in allopatry and preserve within‐species sexual recognition throughout the breeding range. A closer look at the evolutionary history and ecology of these two species illustrates how such a mimetic system can evolve. Although likely rare, this phenomenon might not be unique to Ficedula flycatchers.

Foster, but not genetic, father plumage coloration has a temperature-dependent effect on offspring quality

Secondary sexual characters have most likely evolved through sexual selection because such traits indicate the genetic or phenotypic quality of the bearer. While genetic variation in such fitness-related traits should be depleted by directional selection, there are many cases in which variation is higher than expected. One hypothesis explaining this variation is that different phenotypes within a population are adapted to different environmental conditions. We tested this hypothesis by comparing the offspring quality of male pied flycatchers, Ficedula hypoleuca, with different degrees of melanin-based dorsal plumage coloration under different environmental conditions. To create different environmental growth conditions and to be able to separate offspring genotype effects from paternal effects on offspring body mass, we used a partial cross-foster design where the brood size was reduced or enlarged by one chick. We also examined the interactive effects of temperature and male phenotype because previous correlative studies suggest such temperature-dependent effects in this species. We show that, while manipulated brood size did not interact with male phenotype to affect offspring quality, temperature during the nestling period influenced the offspring quality of dark and brown foster (but not genetic) fathers. When the temperature was relatively low during the nestling period, foster offspring of black males were lighter than those raised by brown males; the opposite was true if temperature was relatively high. These results add a new aspect to our understanding of how variation in the degree of melanin-based coloration is maintained in wild populations and how phenotypic variation may be maintained in general.

Carry‐over effects of conditions at the wintering grounds on breeding plumage signals in a migratory bird: roles of phenotypic plasticity and selection

To understand the consequences of ever‐changing environment on the dynamics of phenotypic traits, distinguishing between selection processes and individual plasticity is crucial. We examined individual consistency/plasticity in several male secondary sexual traits expressed during the breeding season (white wing and forehead patch size, UV reflectance of white wing patch and dorsal melanin coloration) in a migratory pied flycatcher (Ficedula hypoleuca) population over an 11‐year period. Furthermore, we studied carry‐over effects of three environmental variables (NAO, a climatic index; NDVI, a vegetation index; and rainfall) at the wintering grounds (during prebreeding moult) on the expression of these breeding plumage traits of pied flycatcher males at individual and population levels. Whereas NAO correlates negatively with moisture in West Africa, NDVI correlates positively with primary production. Forehead patch size and melanin coloration were highly consistent within individuals among years, whereas the consistency of the other two traits was moderate. Wing patch size decreased with higher NAO and increased with higher rainfall and NDVI at the individual level. Interestingly, small‐patched males suffered lower survival during high NAO winters than large‐patched males, and vice versa during low NAO winters. These counteracting processes meant that the individual‐level change was masked at the population level where no relationship was found. Our results provide a good example of how variation in the phenotypic composition of a natural population can be a result of both environment‐dependent individual plasticity and short‐term microevolution. Moreover, when plasticity and viability selection operate simultaneously, their impacts on population composition may not be evident.

Sex-dependent responses to increased parental effort in the pied flycatcher

The optimal number of offspring for males and females may differ, as males and females invest differently in different aspects of reproduction. This creates potential for a sexual conflict leading to reduced residual reproductive value of the sex that experiences exploitation by the other sex. We experimentally investigated (by changing the brood size by one offspring) the effects of increased or decreased parental effort on the future local survival and breeding success of adult pied flycatchers (Ficedula hypoleuca), and on the future expression of male ornamentation. In addition, we studied how experimentally changing the brood size affected offspring condition and their recruitment. We show that females (but not males) rearing enlarged broods had lower local survival compared to those rearing reduced or control broods. This indicates a sexual conflict concerning optimal brood size. However, even though brood size manipulation did not affect the local survival of males, it did have an influence on the dorsal melanin coloration of young males. Young males rearing enlarged broods showed a stronger increase in plumage darkness from the current to the next breeding season than those rearing reduced or control broods. This suggests that stress experienced during reproduction might have carry-over effects that influence the complicated melanocortin system and lead to changes in the expression of melanin-based coloration. Alternatively, successful breeding might have stimulated young males to further invest in reproduction in the following season. Taken together these results indicate that both sexes are affected by brood demands, but in different ways.

Nosy neighbours: large broods attract more visitors. A field experiment in the pied flycatcher, Ficedula hypoleuca

Life is uncertain. To reduce uncertainty and make adaptive decisions, individuals need to collect information. Individuals often visit the breeding sites of their conspecifics (i.e., “prospect”), likely to assess conspecifics’ reproductive success and to use such information to identify high-quality spots for future breeding. We investigated whether visitation rate by prospectors and success of visited sites are causally linked. We manipulated the reproductive success (enlarged, reduced, and control broods) in a nest-box population of migratory pied flycatchers, Ficedula hypoleuca, in Finland. We measured the visitation rates of prospectors at 87 nest-boxes continuously from manipulation (day 3 after hatching) to fledging. 302 adult pied flycatchers prospected 9194 times on these manipulated nests (at least 78% of detected prospectors were successful breeders). While the number of visitors and visits was not influenced by the relative change in brood size we induced, the resulting absolute brood size predicted the prospecting behaviour: the larger the brood size after manipulation, the more visitors and visits a nest had. The parental provisioning rate at a nest and brood size pre-manipulation did not predict the number of visitors or visits post-manipulation. More visitors, however, inspected early than late nests and broods in good condition. Our study suggests that individuals collect social information when visiting conspecific nests during breeding and provides evidence that large broods attract more visitors than small broods. We discuss the results in light of individual decision-making by animals in their natural environments.

Fungal spore diversity reflects substrate-specific deposition challenges

Sexual spores are important for the dispersal and population dynamics of fungi. They show remarkable morphological diversity, but the underlying forces driving spore evolution are poorly known. We investigated whether trophic status and substrate associations are associated with morphology in 787 macrofungal genera. We show that both spore size and ornamentation are associated with trophic specialization, so that large and ornamented spores are more probable in ectomycorrhizal than in saprotrophic genera. This suggests that spore ornamentation facilitates attachment to arthropod vectors, which ectomycorrhizal species may need to reach lower soil layers. Elongated spore shapes are more common in saprotrophic taxa, and genera associated with above ground substrates are more likely to have allantoid (curved elongated) spores, probably to lower the risk of wash out by precipitation. Overall, our results suggest that safe arrival on specific substrates is a more important driver of evolution in spore morphology than dispersal per se.

Predator encounters have spatially extensive impacts on parental behaviour in a breeding bird community

Predation risk has negative indirect effects on prey fitness, partly mediated through changes in behaviour. Evidence that individuals gather social information from other members of the population suggests that events in a community may impact the behaviour of distant individuals. However, spatially wide-ranging impacts on individual behaviour caused by a predator encounter elsewhere in a community have not been documented before. We investigated the effect of a predator encounter (hawk model presented at a focal nest) on the parental behaviour of pied flycatchers (Ficedula hypoleuca), both at the focal nest and at nearby nests different distances from the predator encounter. We show that nest visitation of both focal pairs and nearby pairs were affected, up to 3 h and 1 h, respectively. Parents also appeared to compensate initial disrupted feeding by later increasing nest visitation rates. This is the first evidence showing that the behaviour of nearby pairs was affected away from an immediate source of risk. Our results indicate that the impacts of short-term predator encounters may immediately extend spatially to the broader community, affecting the behaviour of distant individuals. Information about predators is probably quickly spread by cues such as intra- and heterospecific alarm calls, in communities of different taxa.

Severe effects of long-term drought on calcareous grassland seed banks

Climate change models project shifts in precipitation patterns at regional and global scales. Increases in dry areas and the occurrence of drought predicted in future scenarios are likely to threaten grassland ecosystems. Calcareous grassland seed banks have proven to be resistant to short-term drought, but their responses to long-term drought are unknown. Here we show that 14 years of summer drought changed calcareous grassland seed bank composition, reducing its size and richness, and that these responses do not simply reflect patterns in the above-ground vegetation. Moreover, the effect of drought was larger on seed banks than on vegetation, and above-ground responses mediated by soil depth were less evident in the seed bank than in the vegetation. These results demonstrate that the severity of drought effects on calcareous grasslands is larger than previously thought, and show that this ecosystem is highly vulnerable and has low resilience to predicted decreases in soil moisture.Drought: grassland biodiversity reservoirs are at risk!Long-term drought severely reduces the size and richness of the soil seed bank beneath calcareous grassland. Sofía Basto at the Universidad Javeriana, Colombia, and collaborators worlwide, demonstrated that negative effects of drought are larger on seed banks than on vegetation by sampling soils after 14 years of experimental drought, and simulating future climate change scenarios. Although drought-sensitive species decreased both above and below ground, several species disappeared from the seed bank. This is of concern because seed banks help to maintain vegetation diversity, reduce extinction risk, and allow recovery after disturbance. Understanding the mechanisms responsible for this decline is crucial to predict the vulnerability of grasslands under the increase in drought frequency and intensity detected worldwide.