Patterns of annual and seasonal immune investment in a temporal reproductive opportunist

Abstract

Historically, investigations of how organismal investments in immunity fluctuate in response to environmental and physiological changes have focused on seasonally breeding organisms that confine reproduction to seasons with relatively unchallenging environmental conditions and abundant resources. The red crossbill, Loxia curvirostra , is a songbird that can breed opportunistically if conifer seeds are abundant, on both short, cold, and long, warm days, providing an ideal system to investigate environmental and reproductive effects on immunity. In this study, we measured inter- and intra-annual variation in complement, natural antibodies, PIT54 and leucocytes in crossbills across four summers (2010–2013) and multiple seasons within 1 year (summer 2011–spring 2012). Overall, we observed substantial changes in crossbill immune investment among summers, with interannual variation driven largely by food resources, while variation across multiple seasons within a single cone year was less pronounced and lacked a dominant predictor of immune investment. However, we found weak evidence that physiological processes (e.g. reproductive condition, moult) or abiotic factors (e.g. temperature, precipitation) affect immune investment. Collectively, this study suggests that a reproductively flexible organism may be able to invest in both reproduction and survival-related processes, potentially by exploiting rich patches with abundant resources. More broadly, these results emphasize the need for more longitudinal studies of trade-offs associated with immune investment.

Immune function differs among tropical environments but is not downregulated during reproduction in three year-round breeding equatorial lark populations

“…A small clutch size may allow red-capped larks to simultaneously maintain both reproduction and immune function. Long lived birds with a slower pace of life are associated with well-developed immune defences (Martin et al 2006 ; Lee et al 2008 ) and are known to favour investments that increase survival, including immune defenses, even under challenging conditions such as reproduction (Tella et al 2002 ; Ardia 2005 ; Lee 2006 ; Lee et al 2008 ; Tieleman et al 2019 ; Schultz et al 2020 ). On the other hand, birds in mid-to-high latitudes are short-lived and have a faster pace of life and supposedly invest in reproduction (large clutch size) at the expense of self-maintenance (Martin et al 2006 ; Lee et al 2008 ).…”

“…Our findings suggest that different immune indices were differently influenced by environmental conditions using location as proxy for different climatic conditions. Temperature (Shephard et al 1998 ; Bowden et al 2007 ; Schultz et al 2020 ) and rainfall (Rubenstein et al 2008 ; Schultz et al 2020 ) have been shown to influence different components of immune function. Moreover, temperature (Watts et al 1987 ; Demas and Nelson 1998 ; Altizer et al 2006 ; Lowen et al 2007 ) and rainfall (Bicout and Sabatier 2004 ; Tieleman et al 2019 ) can influence both the broader geographical patterns and the short-term local dynamics of pathogens and diseases, which would be expected to drive immunological variation (Christe et al 2001 ; Møller et al 2003 ; Horrocks et al 2012b ; Tieleman et al 2019 ; Schultz et al 2020 ).…”

“…Seasonal variation in constitutive innate immune function in birds from temperate and arctic zones has been attributed to such trade-offs (Martin et al 2008 ; Hegemann et al 2012a ). Yet other studies provide contrary evidence showing that immune function is maintained in the face of reproduction (Tieleman et al 2019 ; Schultz et al 2020 ) and other supposedly competing physiological processes, e.g., endocrinological changes (e.g. Vindevogel et al 1985 ; Allander and Sundberg 1997 ; Christe et al 2000 ; Møller et al 2003 ; Alonso-Alvarez et al 2007 ).…”

“…Immune function also varies with the abiotic conditions of an animal’s environment (Lowen et al 2007 ; Rubenstein et al 2008 ; Sehgal et al 2011 ; Horrocks et al 2012b , 2015 ; Zamora-Vilchis et al 2012 ; Schultz et al 2020 ), and a single species can mount different immune responses depending on geographical location (Ardia 2007 ). This type of immunological variation may reflect resource availability, “pathogen pressure”, or some combination of the two (Schultz et al 2020 ; van Veelen et al 2020 ).…”

“…Immune function also varies with the abiotic conditions of an animal’s environment (Lowen et al 2007 ; Rubenstein et al 2008 ; Sehgal et al 2011 ; Horrocks et al 2012b , 2015 ; Zamora-Vilchis et al 2012 ; Schultz et al 2020 ), and a single species can mount different immune responses depending on geographical location (Ardia 2007 ). This type of immunological variation may reflect resource availability, “pathogen pressure”, or some combination of the two (Schultz et al 2020 ; van Veelen et al 2020 ). Pathogen pressure encompasses the abundance and diversity of parasites, pathogens, and even commensal microorganisms in the environment (Sheldon and Verhulst 1996 ; Christe et al 2001 ; Møller et al 2003 ; Tschirren and Richner 2006 ; Horrocks et al 2011 , 2012b ) and on the animal itself (Horrocks et al 2012a ).…”