Introduction
Nests are fundamental structures for avian reproduction that determine egg survival and development (Deeming et al. 1991; Deeming & Mainwaring 2015). The thermal environment inside these natural incubators influences an individual’s fitness, and therefore, nest traits that affect internal conditions are expected to be under strong selective pressures (Heenan 2013; Mainwaring et al. 2014). Songbirds (suborder Passeri) and their more than 4500 species represent the largest extant bird radiation and are known to build a variety of nest types. The majority of species in this clade build ‘open nests’, that is, cups or platforms where nest contents are exposed. In contrast, some species, like Australian lyrebirds, African weavers and penduline tits, build domed nests, which are structures characterised by an enclosing roof and a side entrance. Domed nests have often been suggested to reduce predation and offer thermal insulation, protecting nest contents better than open nests (Collias 1997; Lamprecht & Schmolz 2004; Martin et al. 2017). Recent evidence highlights their thermoregulatory advantages in colder environments by enabling parents to spend more time away from their nests (Lamprecht & Schmolz 2004; Martin et al. 2017; Matysioková & Remeš 2018), and in extremely hot environments by shielding nests from solar radiation (Griffithet al. 2016). Given the presumed advantages of domed nests over open nests, it remains a mystery why most birds in the world (~70% of all avian families, 72% of songbird species) build open nests.
For years it was thought that selective pressures, imposed by temperature or predation rates, would have favoured the transition from open to domed nests in some clades (Collias 1997; Hansell 2000; Price & Griffith 2017). The evolutionary history of nests in passerines, however, suggests the opposite: the common trait of building an open nest is a derived condition, an innovation. In 2017, Price and Griffith found evidence that the ancestral type of nest in passerines is domed, and this result is further supported by other comparative analyses (Fanget al. 2018; Medina 2019). Thus, rather than selection favouring the occurrence of domed nests throughout the evolution of passerines, this trait has been repeatedly lost. Furthermore, the transition from domed to open nests in passerines has been hypothesized to be a key innovation, given the subsequent diversification, colonization and expansion of open nest building lineages (Price & Griffith 2017; Fanget al. 2018). We currently ignore why domed nests transitioned into open structures, but it is possible that costs associated with nest building could have led to the repeated loss of domed nests. For instance, while we lack information on whether building domed nests represents a higher energetic cost over building open nests, nest building is considered a costly activity and domed nests are heavier relative to the size of the builder when compared to open nests (Hansell 2000; Mainwaring & Hartley 2013). Yet, we still lack formal analyses at large taxonomic scales to understand the underlying evolutionary processes and life-history implications of the transition between domed and open nests.
The type of nest a species builds could be tightly linked with its ability to live across different habitats or environments. For instance, if domed nests offer greater protection across a wider range of environments, then we would expect species with domed nests to sustain broader climatic tolerances, thereby enabling them to inhabit a wider range of habitats. On the other hand, if domed nests are a costly ancestral adaptation to now scarce specific habitats, then domed-nest lineages should exhibit narrower and more specialized environmental tolerances than their open-nest counterparts. An increased availability of milder habitats (in terms of climate and/or predation) could have released lineages from the costs of domed nest-building, resulting in larger populations and larger ranges, and potentially, an increase in speciation or reduction in extinction rates (Rosenzweig 1995). Indeed, Australian species with open nests tend to have larger ranges, wider climatic niches and are less likely to be under an IUCN threat category compared with species that build domed nests (Medina 2019).
Our main aim is to understand the evolutionary success of open nests by studying the potential ecological and evolutionary trade-offs associated with different nest types. First, we compare the building costs between domed and open nests using published information on time spent constructing the nest. We then test whether the evolution of domed and open nests in passerines is associated with differences in range size, climatic niche breadth, colonisation of novel environments and differences in speciation or extinction rates. We use a comprehensive macroevolutionary framework to explore for the first time the joint evolutionary dynamics of a critical component of the extended phenotype of birds.