Adaptation and constraint shape the evolution of growth patterns in passerine birds across the globe

Abstract

Background: Growth trajectories should be adapted to selective factors of each species' environment. However, major shaping forces of growth and development are unclear, especially when studying several traits at once. Birds provide an ideal opportunity to analyze growth patterns across species due to there being enough available data. We tested the relative importance of nest predation risk, the number of care-givers, nest height, foraging substrate, clutch size, and latitude on growth patterns of passerine birds (Passeriformes) using phylogenetic comparative methods. Specifically, we studied the evolution of fledging time, average and peak growth rates, and relative development at fledging of body mass and tarsus, wing, and tail length.

Results: Using a comprehensive literature search and data quality control, we obtained data on growth in 231 species based on 295 populations. Species with long development in the nest grew slowly and had well-developed traits at fledging. Species breeding under high nest predation risk, building their nests close to the ground, and those living in northern temperate regions fledged early and grew fast, sometimes fledging with less developed body mass and traits critical for locomotion (tarsus, wing, and tail). On the other hand, the number of caring adults, clutch size, and species' foraging substrate had very limited predictive value for growth patterns across passerine species.

Conclusions: Shortening of the nestling period was a primary means of accelerating development (in relation to nest predation, nest height, and latitude), sometimes supplemented by higher peak growth rates of body mass, tarsus, and wing (especially in relation to latitude). Overall growth patterns of passerines were adaptively tuned to nest predation risk and nest height, with northern temperate species having especially short nestling periods and fast growth rates of body mass, tarsus, and wing.

Keywords: Birds; Development; Growth rate; Latitude; Life history; Nest predation.

Fig. 1

Relative development of traits at fledging (top) and peak growth rates (bottom) in relation to fledging age in passerines. In relative trait development, the value of 1 means that the trait was developed at 100% of adult value at fledging, and this is designated by a horizontal line. Growth rate is the peak growth rate (K parameter) from a sigmoid growth model (either three-parameter U-Logistic or four-parameter U-Richards model). There are two lines for mass growth (for both Logistic and Richards models); one is for complete nestling data, while the other is for nestling body mass truncated at 70% of adult mass. These relationships remained unchanged when growth rates and fledging age were adjusted for allometry (see Figs. S12–S17 in Additional File 2 and Tables S4 and S5 in Additional File 1)

Fig. 2

Relationships between traits characterizing growth patterns of passerines (relative size and mass at fledging, fledging age, and growth rates) and most important predictors (nest predation risk, nest height, and absolute geographic latitude). For statistics, see Tables S7–S12 in Additional File 1

Fig. 3

Summary of relationships among predictors (yellow rectangles) and dependent variables (grey ovals). Models were fit using phylogenetic generalized least squares regressions. Effect size is a standardized regression coefficient and is depicted by path width. We did not use phylogenetic path analyses, because that would lead to substantially reduced sample sizes. “Growth rate” is peak growth rate (U-Logistic curve) and it was not estimated for tail length (see Methods). “Latitude” is a geographic latitude, increasing away from the equator. For statistics, see Tables S7–S12 in Additional File 1

Fig. 4

Growth rates of passerine nestlings in relation to latitude, expressed as geographic bands delimited by the Tropic of Capricorn (23.5°S) and Tropic of Cancer (23.5°N). “Southern” means south of 23.5°S, “Northern” means north of 23.5°N, while “Tropical” means between the two Tropics. For statistics, see Tables S10–S12 in Additional File 1

Fig. 5

Evolutionary responses of growth in passerines to ecological factors. The strongest response to high nest predation risk, building nests close to ground, and living in northern temperate latitudes is shortening of fledging age (red arrow from FA1 to FA2). Due to the sigmoid shape of typical growth trajectory, this brings only a small decrease in relative fledging traits (from FT1 to FT2). However, due to a strong response in fledging age, it is tied to strong increase in average growth rate (where fledging age is in the denominator of the formula for its calculation). Finally, peak growth (slope of a tangent of the growth curve at the inflection point, depicted here as a red line) is sometimes also higher (increase from K1 to K2), especially for the latitudinal effect (see Figs. 2 and 3). Also note that longer fledging age (FA1 > FA2) is correlated with slower peak growth (K1 < K2) and larger fledging traits (FT1 > FT2, see Fig. 1)