The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models

Abstract

Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and / or among clutches. Here we tested for such correlations between maternallyderived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology. Egg components are important mediators of prenatal maternal effects in birds 28 and other oviparous species. Because different egg components can have 29 opposite effects on offspring phenotype, selection is expected to favour their 30 mutual adjustment, resulting in a significant covariation between egg 31 components within and / or among clutches. Here we tested for such 32 correlations between maternally-derived yolk immunoglobulins and yolk 33 androgens in great tit (Parus major) eggs using a multivariate mixed model 34 approach. We found no association between yolk immunoglobulins and yolk 35 androgens within clutches, indicating that within clutches the two egg 36 components are deposited independently. Across clutches, however, there 37 was a significant negative relationship between yolk immunoglobulins and 38 yolk androgens, suggesting that selection has co-adjusted their deposition. 39Furthermore, an experimental manipulation of ectoparasite load affected 40 patterns of covariance among egg components. Yolk immunoglobulins are 41 known to play an important role in nestling immune defence shortly after 42 hatching, whereas yolk androgens, although having growth-enhancing effects 43 under many environmental conditions, can be immunosuppressive. We 44 therefore speculate that variation...

The Evolution of Multivariate Maternal Effects

“…For example, the vector z ( t ) may reflect titers of different offspring hormones, and the entry specifies how the maternal titer of hormone j (e.g., measured during pregnancy or added to the egg) affects the titer of offspring hormone i (e.g., mediated by the number of hormone binding sites present in the offspring endocrine cells). Indeed, studies indicate that maternal hormone and protein titers affect offspring hormone concentrations, often in a multivariate fashion (e.g., [33], [56], [69]). …”

“…However, most studies on maternal effects focus mainly on univariate scenarios, in which a single maternal factor influences a single offspring character. By contrast, studies in plants and animals suggest that maternal effects typically have a multivariate nature, involving suites of interacting parental and offspring characters (e.g., [30]–[33]). Indeed, this multivariate nature has long been appreciated by those models that assess the consequences of (non-evolving) nongenetic effects to phenotypic evolution [34]–[38].…”

“…First, as stated before, the main prediction of univariate models is that maternal effects evolve when the parental phenotype correlates with selective conditions encountered by offspring [23], [24], [29], [39]. It is currently unclear how these predictions play out when offspring are not influenced by a single, but multiple components of a parental phenotype, raising the question how offspring should weigh information that results from the presence of multiple maternal effects (e.g., the presence of multiple maternal hormones and immonoglobulins in avian eggs [33], [40], [41]). A second reason for considering the evolution of nongenetic effects in a multivariate context is the finding [42] that the multivariate configuration of all maternal effects (here assumed to be captured in the matrix M , [34], [36], [43]) plays an analogous role in determining the course of evolution as the genetic variance-covariance matrix G that describes the scope for correlated selection between traits [44]–[46].…”

Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

“…It has been hypothesized that females balance the costs and benefits of one component with another. For example, higher levels of immune factors could compensate the immunosuppressing effects of high yolk androgen levels (Royle et al, 2001;Groothuis et al, 2006), but the results of the phenotypic correlations are currently contradictory (Groothuis et al, 2006;Gasparini et al, 2007;Hargitai et al, 2009;Ruuskanen et al, 2011;Postma et al, 2014). On the other hand, yolk hormones A4 and T that are phenotypically correlated have been found to show differential effects in offspring: A4, but not T, decreased growth (Muriel et al, 2013) and A4, but not T, was positively correlated with offspring recruitment (Hegyi et al, 2011;Tschirren et al, 2014).…”

Factors affecting the levels of protection transferred from mother to offspring following immune challenge

“…It is unclear whether females that transfer high levels of one maternal component such as antibodies may also transfer high levels of other key egg components in general. This would warrant further investigation to test if some females generally transfer more of all constituents or whether trade-offs occur (for example, more antibodies may be needed to balance hormonal immuno-mediated effects [28]).…”