Across many taxa, clinal variation in body size has been observed to follow Bergmann's rule, which predicts larger body size in colder climates. For more than a century, this pattern has typically been ascribed to selection for large body size in cold winter climates. Here, in spatially distributed observational data from 30 populations of House Sparrow (Passer domesticus) introduced into Australia and New Zealand, we show that this relationship appears to be explained by a negative relationship with high temperatures during the breeding season. Our results suggest that higher temperatures during the breeding season could reduce body size through developmental plasticity, which should be considered in combination with or as an alternative to selection. Our findings would predict that a hotter climate during breeding could drive significant changes in morphology among populations (and potentially within populations as well, if climate varies temporally across a breeding season). This idea, and our support for it, could account for much of the variation in body size that drives the well-observed patterns first described by Bergmann, and that are still largely attributed to selection on adult body size during cold winters. Understanding the mechanisms behind any climate-dependent developmental plasticity could prove useful for understanding how endotherms may be affected by climate change in the future.
For over 100 years since the publication of Bergmann's rule in 1847 (Bergmann 1847), a clinal pattern of animals having larger body sizes in colder climates has been observed in a majority of the hundreds of species that have been examined (Mayr 1956, James 1970, Ashton et al. 2000, Ashton 2002, Meiri and Dayan 2003, Millien et al. 2006, Clauss et al. 2013, Teplitsky and Millien 2014). To date, most studies still cite Bergmann's original explanation that larger body size is favored by natural selection in colder climates because of the thermoregulatory benefits of a smaller volume to surface area ratio (Briscoe et al. 2015, Cardilini et al. 2016, Salewski and Watt 2017). A classic example of clinal variation in avian body size has previously been demonstrated in North American populations of the introduced House Sparrow (Passer domesticus; Johnston and Selander 1964, 1973, Murphy 1985). If winter temperatures are the selective force responsible for this clinal variation, as predicted by Bergmann's rule, then variation in body size between populations should be best explained by winter minimum temperatures. However, in hotter climates, smaller body size can also be advantageous to an individual's ability to thermoregulate by dissipating heat (Partridge and Coyne 1997), even though the benefits of minor changes in body size within species have been questioned for more than 40 yr (Scholander 1955, McNab 1971).
Understanding the mechanisms that create the morphological differentiation described by Bergmann's rule has gained fresh impetus as part of the study of the effects of a changing climate on animal populations (Gardner et al. 2011). Indeed, declining body size in a number of avian species has been linked to increasing temperatures consistent with climate change (Gardner et al. 2009, Van Buskirk et al. 2010), and it has been suggested that higher temperatures during development may act as an influence on plasticity in growth (Merilä and Hendry 2014). The idea that clines in body size are a result of phenotypic plasticity in morphology that is mediated by the effects of high temperatures on growth is now gaining traction (Teplitsky et al. 2008, Van Buskirk et al. 2010, Yom-Tov and Geffen 2011). In hot climates, nests can potentially act to buffer ambient conditions, but they can still get very hot. Recent work found that Zebra Finch (Taeniopygia guttata) nests in the Australian desert were typically several degrees warmer than ambient conditions and that internal nest temperatures occasionally exceeded 50°C (Griffith et al. 2016). Nest microclimates may therefore be a significant determinant of variation in developmental plasticity and may have the capacity to affect development and growth. Indeed, it has recently been found observationally in a wild population and experimentally in a captive population of the Zebra Finch that higher temperatures during development lead to reduced fledgling and adult body size (Andrew et al. 2017).
If temperature during development is indeed important, then, at the population level, summer maximum temperatures will be a better predictor of mean body size across locations than winter minimum temperatures. As with the House Sparrows studied in North America (Johnston and Selander 1964, 1971, Murphy 1985), the species was deliberately introduced into Australia and New Zealand in the mid-19th century from founders taken from northwestern Europe (Andrew and Griffith 2016). Over the next century, House Sparrows expanded their range to occupy most of the urban areas across both the North and South islands of New Zealand and the eastern half of Australia (Andrew and Griffith 2016), and today are found in a range of climates that are far more variable and extreme than those in the area from which they were sourced. The House Sparrow populations in Australia and New Zealand therefore provide an opportunity to assess the extent to which a species may respond to a changing climate in a relatively short period of time (∼160 yr at most, and <50 yr for the populations at the extreme edge of their range in Australia; Andrew and Griffith 2016). Here, we use these populations of a sedentary avian species (Anderson 2006) to test the extent to which clinal variation in body size is related to both winter minimum and summer maximum temperatures. This will provide new insight into the extent to which body size is a response to the climate experienced during development rather than a response to selection over the winter.