Introduction :
A key question in the study of animal cognition is whether sexual
selection has contributed to its evolution (Darwin 1871; Boogert,
Fawcett, et al. 2011). A related but subtly different question is
whether signals used in mate choice reflect cognitive abilities that are
under natural selection, and would therefore offer direct or indirect
benefits in a potential mate. The extension of this question is whether
the utility of certain assessment signals in selecting a mate with
beneficial cognitive abilities has led to their continued use and
evolution.
The hypothesis that signals used
in mate choice (“assessment signals”) serve as indicators of male
quality has been extensively supported in a wide variety of taxa
(reviewed in Wilgers and Hebets 2015), including fish (Houde and Torio
1992; Karino et al. 2005), birds (Hill 1991; Doucet and Montgomerie
2003), insects (David et al. 2000; Holzer et al. 2003), and even humans
(Hume and Montgomerie 2001; Little et al. 2008). The hypothesis that
assessment signals can serve as an indicator of general brain function
has also been supported (Boogert, Fawcett, et al. 2011), in particular
by studying the effects of developmental stress on bird song (Peters et
al. 2014). Developmental stress lowers cognitive performance in a range
of taxa (Levitsky and Strupp 1995; Erhard et al. 2004; Kitaysky et al.
2006; Santos de Souza et al. 2008; Peters et al. 2014; Kriengwatana et
al. 2015) and, specifically within birds, on a range of tasks including
novel foraging tasks (Kitaysky et al. 2006), spatial learning tasks
(Pravosudov et al. 2005; Kriengwatana et al. 2015), associative learning
tasks (Fisher et al. 2006; Farrell et al. 2016), and auditory learning
tasks (Farrell et al. 2016). Developmental stress also negatively
impacts preferred features of song, such as complexity (Spencer et al.
2003; Buchanan et al. 2004), bout duration (Buchanan et al. 2003), and
accuracy in relation to tutor song (Nowicki et al. 2002), and is less
preferred by females when presented in comparison with song from
developmentally robust males (Spencer et al. 2005; Searcy et al. 2010).
These findings suggest that song can serve as an indicator of gross
brain quality and function in the case of developmental inequity between
potential mates. However, in the absence of conditions like
developmental stress or genetic abnormalities that cause widespread
disruption in the body and brain, there is increasing evidence that
avian intelligence is more modular than general in nature (Searcy and
Nowicki 2019). For instance, there are seldom correlations between
performance on different cognitive tasks within individuals (Nettle et
al. 2015; van Horik and Madden 2016; Anderson et al. 2017; Medina-García
et al. 2017; DuBois et al. 2018; MacKinlay and Shaw 2018), with some
exceptions (Shaw et al. 2015; Ashton et al. 2018). Notably, exceptions
tend to occur in wild populations where unequal developmental conditions
are more likely. Because of the apparent modularity of avian
intelligence, it is unclear whether song is a reliable indicator of the
specific cognitive skills that would offer females fitness benefits if
found in a potential mate.
One such cognitive skill is foraging ability.
Foraging efficiency has been shown
to increase fitness in a range of avian species (Orians 1969; Weathers
and Sullivan 1989; Lemon and Barth 1992; Lescroël et al. 2010; Cole et
al. 2012), and is a particularly important skill in a mate in monogamous
species that engage in biparental food provisioning. Indicative of its
importance, foraging ability has also been shown to directly affect mate
preferences in crossbills (Loxia curvirostra ), budgerigars
(Melopsittacus undulatus ), and zebra finches (Taeniopygia
guttata ) when females directly observe males solving a foraging task
(Chantal et al. 2016; Chen et al. 2019) or more efficiently extracting
food from a source (Snowberg and Benkman 2009; Chantal et al. 2016).
Foraging ability is also correlated with problem-solving on artificial
tasks in the wild (Cole et al. 2012; Cauchard et al. 2013), which has in
turn been correlated with reproductive success (Keagy et al. 2009; Cole
et al. 2012; Cauchard et al. 2013; Ashton et al. 2018).
The ability to solve a novel foraging problem is thus related to
reproductive success and has been shown in some species to be preferred
by females when observed directly. However, it remains unclear whether
the same signals that can indicate gross brain function, as determined
by developmental conditions, can reflect this specific skill. Do songs
contain information about male foraging ability, given the apparent
modularity of avian cognition, and could this help explain the utility
of song as an assessment signal? Or, conversely, does song only contain
information about gross developmental conditions, and not more specific
skills that would offer females direct fitness benefits?
To answer these questions, we tested whether female zebra finches would
discriminate between males with superior versus inferior performance on
a novel foraging task based solely on their song. Using an operant
conditioning assay, we compared female preference for the songs of males
that quickly solved the novel foraging task to the songs of males that
were incapable of solving the task. The females had no exposure to the
males whose songs they were tested with, thus isolating their knowledge
of the males to information contained in their songs. We predicted that
if song is a reliable signal of novel foraging skill, females would be
able to identify and prefer songs from males who were capable of quickly
solving a novel foraging task over songs from males who were unable to
solve the task.