1. Behavioural adaptations in cavity nesting birds.

1.1. Behavioural responses to ectoparasites. Generalist ectoparasites infest nests of avian cavity-nesting passerines as a response to different factors present in host species. Firstly, I found that differences in nest material composition among host species are not the main factor explaining ectoparasite prevalences and abundances, while nest size, breeding phenology, brood size and nest-cavity micro-climate may all affect levels of infestation in different ways for each host-parasite association (Cantarero et al., 2013. Acta Ornithol.). Given the negative impact of ectoparasites on nestlings, there will be selection on hosts to reduce parasite infestations through behavior. I showed that frequency and intensity of female anti-parasite behaviors during the incubation and nestling periods decreased as a consequence of the experimental reduction of ectoparasite infestation and these behaviors were more intense in the host species with highest infestation levels (Cantarero et al., 2013. J. Avian. Biol.) Additionally, nests without any structure such as those built by Nuthatches may offer fewer opportunities for hiding to ectoparasites and nest composition may affect ectoparasite development through the effects of microclimatic conditions associated with different nest materials. I showed that the replacement of unstructured nests by structured nests did not result in changes in ectoparasite loads (Cantarero et al., 2014. Acta Ornithol.), which suggests that the preferences for nest materials in Nuthatches are unrelated to ectoparasitism. We also suggested that Nuthatch nests contribute to reduce the thermal loss for nestlings and possibly eggs during female absences by remaining buried into loose and heat-producing bark flakes.

1.2. Competition for nesting cavities. Given that nesting cavities are a scarce resource, there may be strong competition over them. We found that levels of testosterone differ between populations of the same species, being higher in populations where the likelihood of nest-site usurpation by intruders is greater (Cantarero et al., 2017. J. Avian. Biol.). We also found that the level of female aggressiveness against intruders in high density areas decrease even when showing higher blood T levels (Cantarero et al., 2015. Ethology). After obtaining a nest cavity or nest-box, nest building begins. Some species such as Nuthatches show clear preferences for certain nesting materials and cavities for breeding. The selection of nesting material and the amount of mud in Nuthatch nest-boxes can be explained as a constrain between requirements for nest construction and availability as a function of transport distance (Cantarero et al., 2015. Ardea).

1.3. The evolution of female begging. We firstly showed that nestlings begged more intensely as a response of higher nutritional needs arising from higher ectoparasite loads (Cantarero et al., 2013. J. Avian. Biol.). While begging by nestlings has received a fair deal of attention as an honest system of communication, begging between mates has received scant attention. We tested if female begging during incubation is an honest signal of energetic need. We found that experimentally handicapping female pied flycatchers intensified begging displays arising from condition impairment and that males were able to respond by increasing their feeding rates to females (Cantarero et al., 2014. Anim. Behav.).

2. Sexual conflict.

2.1. Post-mating sexual signals. My studies on the function of non-bodily ornaments (‘extended phenotype’) as sexual sexually selected or status signals have revealed novel aspects regarding how birds can transmit information to the partner and/or conspecifics (potential competitors). We first experimentally demonstrated that nest size constitutes a signal of female quality in nuthatches and thereby, induce males to increase their reproductive investment both to females and to their broods (Cantarero et al., 2016. Behav. Ecol. Sociobiol.). Moreover, we provided evidence that jackdaws use nest decorations in their nests in order to indicate their parental quality, experience or genetic quality and also induce differential resource allocation (Cantarero et al., in preparation).

2.2. Sexual conflict and brood desertion. I combine an understanding of the origin of sexual signals and how they modulate the outcome of conflicts within the pair. I explored the role of male and female attractiveness on nestling sex ratio (Cantarero et al., 2018. J. Avian. Biol.) and showed that brood sex ratios were predicted by the interaction of male and female ornaments. Moreover, other study showed that members of a pair do not make independent decisions, but negotiate to modify their effort in direct response to the prior effort of their mate (Cantarero et al., 2019. Behav. Ecol. Sociobiol.).

2.3. Spatiotemporal patterns of extra-pair paternity. In tight connection with the previous point, I have been interested in the socio-ecological factors determining extra-pair paternity (EPP) in songbirds, a neglected topic in the literature. Through several experimental studies in pied flycatchers, we have demonstrated the importance of individual characteristics of both males and females on the one hand, and the influence of the social context on the other in determining the resulting behavioural reproductive patterns (Among others, Plaza et al., 2018. Behav. Ecol. Sociobiol., Plaza et al., 2019. Biol Lett.).

3. Carotenoid-based ornaments and sexual selection.

3.1 Ornamental traits involved in sexual selection. Sexual selection promotes the evolution of conspicuous animal ornaments. To evolve as signals, these traits must reliably express the “quality” of the bearer, an indicator of individual fitness. We showed that carotenoid-based plumage traits signal parental quality in female Rock sparrows (Cantarero et al., 2017. Etho. Ecol. Evol.) and male longevity and lifetime fecundity in red-legged partridges, the latter requiring a tightly-controlled steroid metabolism to transmit this information reliably (Cantarero et al., 2019. Plos One). Moreover, many species also develop complex body designs (shapes, drawings) that could have a role as visual signals during courtship and social interactions, but an empirical validation in the wild is currently lacking. Our research in red-legged partridges provided the first evidence in the wild of a relationship between the complexity of a pigmented pattern and assortative mating and mating success, suggesting that this type of ornament could be the product of sexual selection (Cantarero et al., 2019. The Science of Nature).

3.2 Mechanisms involved in the expression of carotenoid-based ornaments. In the context of this project, I focused my attention on the study of the mechanisms involved in the expression of sexual signals generated by red carotenoid pigments and the role of the mitochondria in this process. Some authors recently suggested that a certain type of carotenoid-based signal (those produced by red pigments obtained by transforming yellow carotenoids) could have evolved as index signals without production costs, revealing individual quality by its intrinsic (constraining) link to individual physiology. They suggested that red carotenoid-based colorations could only be produced by an efficient cell respiration at the mitochondria as the enzymes involved in carotenoid transformations could be placed into the inner mitochondrial membrane (IMM). This hypothesis was named the shared hypothesis pathway hypothesis (“SPH”; Hill 2011 Ecol Lett; Johnson and Hill 2013 Biochimie). In this context, I stimulated and inhibited respiratory chain complexes by exposing birds to different compounds under captivity, analyzing its impact on sexual colorations and carotenoid composition/levels. Our first results provided evidence that the hypothetical enzymes responsible for yellow-to red carotenoid transformations (ketolases) are indeed located in or related to the inner mitochondrial membrane (Cantarero et al., 2017. Biol. Lett.). We also showed that the experimental effect of mitochondria-targeted (specifically designed) antioxidants on yellow-to red carotenoid transformations and plumage coloration depends on individual quality determined by the pre-existing coloration level (Cantarero et al., 2020. Evolution). We finally demonstrated for the first time that red coloration and gene expression level of the recently proposed candidate enzyme responsible for converting dietary yellow carotenoids to red ketocarotenoids (i.e. CYP2J19) are both affected by a mitochondria-targeted antioxidant and also by thyroid hormones (Cantarero et al., 2020. Proc. R. Soc. Lond.). This reveals that red (keto)carotenoid based ornaments present in many taxa could depend on mitochondrial function but also be plastic due to hormonal control.

Main ongoing research line and future directions:

4. Carotenoid-based colorations and signalling theory - My current research line is focused on the old hypothesis suggesting that mechanisms at the basis of carotenoid-based ornament expression present in many taxa should primarily be related to evolutionary trade-offs and, therefore, involve production/maintenance costs. 

5. Resolving sexual conflict: mechanisms and evolutionary consequences of parental cooperation.