Testing the strength and direction of selection on vocal frequency using metabolic scaling theory

Abstract

A major challenge for studies assessing drivers of phenotypic divergence is the statistical comparison of taxa with unique, often unknown, evolutionary histories, and for which there are no clear expected trait values. Because many traits are fundamentally constrained by energy availability, we suggest that trait values predicted by scaling theories such as the metabolic theory of ecology (MTE) can provide baseline expectations. Here, we introduce a metabolic scaling-based approach to test theory involving the direction and magnitude of ecological and sexual selection, using vocal frequency as an example target of selection. First, we demonstrate that MTE predicts the relationship between the natural log of body size and natural log of vocal frequency across 795 bird species, controlling for phylogeny. Family-wide deviations in slope and intercepts from MTE estimates reveal taxa with potentially important differences in physiology or natural history. Further, species-level frequency deviations from MTE expectations are predicted by factors related to ecological and sexual selection and, in some cases, provide evidence that differs from current understanding of the direction of selection and identity of ecological selective agents. For example, our approach lends additional support to the findings from many cross-habitat studies that suggest that dense vegetation selects for lower frequency signals. However, our analysis also suggests that birds in non-forested environments vocalize at frequencies higher than expected based on MTE, prompting intriguing questions about the selective forces in non-forest environments that may act on vocal frequency. Additionally, vocal frequency deviates more strongly from MTE expectations among species with smaller repertoires and those with low levels of sexual dichromatism, complicating the use of these common sexual selection surrogates. Broad application of our metabolic scaling approach might provide an important complementary approach to understanding how selection shapes phenotypic evolution by offering a common baseline across studies and taxa and providing the basis to explore evolutionary trade-offs within and among multicomponent and multimodal traits.

The broken-wing display across birds and the conditions for its evolution

“…As a proxy for agents of selection that vary with latitude, we used the absolute value of either the minimum or maximum latitude, whichever was larger. This measure has the advantage that it cannot result in an uninhabited location, which can occur with species with discontinuous ranges when a midpoint is used [ 20 ].…”

Background Acoustics in Terrestrial Ecology

“…Although it is unclear whether sources of noise in these studies elevated sounds above ambient conditions at a scale relevant to breeding birds, unchanged distributions with respect to noise exposure could be explained by habitat filtering by vocal frequency. Several studies suggest that birds that inhabit grasslands and other open environments have higher-frequency vocalizations than would be expected on the basis of allometric scaling alone (Francis & Wilkins 2021) or in comparison to birds in more densely vegetated environments (Weir et al 2012; but see Mikula et al 2021). Whether this vocal trait could explain the absence of responses among grassland birds is an open question; however, highfrequency singing as a preadaptation to areas characterized by noise has support elsewhere.…”

“…Avoidance of noise (gray) by Woodhouse's scrub jays (blue) increases nest success in songbirds (brown) via lower rates of nest predation by jays (Francis et al 2009) and increases densities of black-chinned hummingbirds (purple), which strongly avoid jays when nesting (Greeney et al 2015). Elevated densities of hummingbirds increase pollination of hummingbird-pollinated plants (red) (Francis et al 2012), yet the avoidance of noise by jays negatively affects recruitment of piñon pine (green) (Francis et al 2021), a woodland foundational species that receives seed dispersal services from jays.…”

Disentangling the mechanisms of signal evolution in Tyrannidae flycatchers, part I: song is constrained by morphology and covaries with ecological factors

“…Recent studies on song frequency across over 5000 passerine species found that although there is evidence supporting a relationship between song frequency and body mass, there is no generalized relationship between song frequency and habitat (Mikula et al 2020). These results suggest that variation in passerine song frequency may be primarily driven by selection for morphology, rather than habitat-related selection on sound (Mikula et al 2020, Francis andWilkins 2021); however, recent evidence supports sensory drive within species (Sebastianelli et al 2022). Part of the reason for the mixed results of sensory drive is that previous studies are unclear on what portion of the hypothesis they are testing (Cummings and Endler 2018).…”