Abstract
Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro‐evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α‐dihydrotestosterone [5α‐DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex‐dependent for T); (c) greater among‐female variation of yolk T and 5α‐DHT concentrations in the forest than city population, but similar within‐clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population‐specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone‐mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population‐specific relationships rather than trade‐off against each other.
Highlights
Animals inhabiting urban environments are characterized by marked differences in morphology, physiology, and behavior from conspecifics living in less urbanized habitats (Alberti et al, 2017)
To address whether androgen-mediated maternal effects contribute to the development of phenotype differences between individuals of city and forest populations of European blackbirds, we investigated, as a first step, if exposure of the embryo to maternal androgens in the eggs differs between the populations
Our comparison of yolk androgens and yolk immunoglobulins between city and forest European blackbirds exposed the following patterns: (a) Yolk androgen concentrations were higher in eggs of the forest than the city population; (b) among-clutch variation of yolk androgens was higher in the forest than city population, while within-clutch variation was similar; (c) IgY concentrations were similar and exhibited seasonal decline in both populations; and (d) yolk A4 and T concentrations were positively correlated with IgY concentrations in the city, while negative tendencies were found in the forest population
Summary
Animals inhabiting urban environments are characterized by marked differences in morphology, physiology, and behavior from conspecifics living in less urbanized habitats (Alberti et al, 2017). These alterations could be the result of genetic drift, local adaptation, immigrant selection, and phenotypic plasticity (Johnson & MunshiSouth, 2017; Partecke, 2014). While common garden studies have shown that differences in some behavioral, physiological, and life history traits between city and forest individuals are intrinsic, excluding phenotypic plasticity as the primary explanatory mechanism (Atwell et al, 2012; Costantini, Greives, Hau, & Partecke, 2014; Miranda, Schielzeth, Sonntag, & Partecke, 2013; Partecke & Gwinner, 2007; Partecke, Schwabl, & Gwinner, 2006), these studies cannot rule out maternal effects and organizational effects during development. Environmental conditions known to influence the concentrations of androgens in the avian egg include breeding density (e.g., Duckworth, Belloni, & Anderson, 2015), nest predation risk (e.g., Schwabl, Mock, & Gieg, 1997), parasite prevalence (e.g., Tschirren, Richner, & Schwabl, 2004), and food abundance (e.g., Morosinotto et al, 2016; Verboven, Monaghan, Evans, & Schwabl, 2003), all of which factors often differ starkly between urban and more natural habitats (Shochat, Warren, Faeth, McIntyre, & Hope, 2006)
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