Diversification of Life Histories in New World Birds

LIFE HISTORIES ARE sets of adaptations that improve the match between an organism and its environment. The adaptations are genetic and interact with environmental factors that influence the fitness of the individual and, by extension, the demography of the population to which that individual belongs (Stearns 1992, Roff 2002). Thus, physiological and behavioral attributes of an individual influence the demographic rates of its population. These demographic rates can, in turn, influence the selective advantage of different combinations of attributes, for example through densitydependent feedback mechanisms (Ricklefs 2000a). These feedback mechanisms are then another component of the environment that applies selective pressure on the behavioral and physiological attributes of life histories. Gaining an understanding of how and why life histories vary among populations and species and across environmental gradients has attracted ornithologists for many decades, but significant methodological limitations have focused most of our efforts on a small number of issues, such as the importance of nest predation in shaping life-history strategies (Martin et al. 2000a, b; Ghalambor and Martin 2001). Ornithologists were among the first to recognize geographic patterns in life-history attributes (Lack 1947). Perhaps the most famous example is latitudinal variation in clutch size of songbirds: birds that nest at lower latitudes tend to lay fewer eggs per nest than birds that nest at higher latitudes (Moreau 1944, Skutch 1949). The search for explanations of these interesting patterns led to many studies that evaluated possible mechanisms such as variation in food availability, adult survival rates, and rates of reproductive failure as a function of latitude (Ricklefs 1969, 1977; Martin 1987, 1996). In the process, we identified contrasts between temperate and tropical living, such as greater average longevity and apparently lower investment in single reproductive attempts in tropical areas, compared with shorter lifespans and higher contributions to individual reproductive events in temperate areas. These contrasting strategies are now generally referred to as “pace-of-life” strategies (Ricklefs and Wikelski 2002). Many tropical birds are on the slow end of an axis of continual variation, and many temperate birds tend to be on the fast end. The occurrence of this slow—fast life-history axis might suggest constraints on patterns of variation (Charnov 1993). Indeed, certain combinations of traits frequently co-occur, whereas other combinations are rarely or never observed in nature. For example, species on the slow end of the axis often exhibit lower metabolic rates, slower growth and development, lower nesting success, and longer life spans, whereas those on the fast end tend to show opposite patterns (Martin 1996, Magrath et al. 2000). Examples of attributes that rarely co-occur include species that simultaneously maximize offspring number and adult longevity or offspring number and offspring size. The latter patterns have revealed important tradeoffs in life-history strategies, because multiple energetically expensive activities cannot all be maximized at once (Reznick 1985, Stearns 1989). Investigations into the mechanisms that control these tradeoffs have historically focused on constraints, because the underlying physiological or hormonal components that transduce environmental information into behavioral action were thought to form complexes that restricted the range of possible outcomes available to selection (Finch and Rose 1995). Recently, however, it has been suggested that selection may influence linkages between components that have been considered inseparable (Hau 2007). These connections between the environment and how individuals can respond to environmental information will shape our understanding of life histories in the coming years. Because organismal functions are broadly interconnected, understanding the evolution of life histories requires measurement of key attributes of many different systems. Until recently, we have lacked sufficient data for multispecies comparisons of energy metabolism, immune function, endocrine control mechanisms, stress responses, and some behavioral components of parental investment. Over the past 10 years, new data that describe these attributes have accumulated rapidly. Many of these contributions have been achieved by focusing on a common set of species matched across sites to reduce the effects of phylogenetic differences and then bringing together a group of scientists with multidisciplinary expertise. Our life history—physiology nexus group, which includes all the authors of this paper and other colleagues, is one such group. Here, we summarize recent advances by some of these collaborations in studies of life-history attributes, as well as current information on variation in adult survival across latitudes, before briefly summarizing what studies of avian life histories may tell us about life histories in general. We conclude by charting some promising future directions in studies of avian life histories. The finding that vertebrate life histories can readily be mapped on a one-dimensional slow—fast continuum implies the existence of general constraints that prevent the diversification of life histories in other dimensions (Ricklefs 2000a, Ricklefs and Wikelski 2002). What are the physiological mechanisms that underlie lifehistory tradeoffs? Hormones are internal signaling molecules that are involved in regulating (1) life-history traits such as fecundity, for example by regulation of clutch and egg size (Sinervo and Licht 1991, Sinervo and Svensson 1998), courtship, and parental behavior (Ketterson et al. 1992, Angelier et al. 2009); and (2) processes that determine survival rate, such as immune function, stress and fight-or-flight responses, and many others (Sapolsky et al. 2000, Romero 2004). Recent studies in birds have indicated that the two steroid hormones testosterone and corticosterone are involved in mediating tradeoffs, especially those between fecundity and survival. Testosterone is a steroid hormone found at elevated concentrations in male vertebrates during the breeding season (Knobil and Neill 1988; female vertebrates also produce it, but at lower levels). During the breeding season, increased testosterone concentrations are known to support male reproductive functions and behaviors. Indeed, a long-term study of free-living Dark-eyed Juncos (Junco hyemalis) showed that males with experimentally increased testosterone concentrations had larger home ranges and more extrapair fertilizations than controls (Ketterson et al. 1996). However, testosterone administration in this species decreased the male survival rate (Ketterson et al. 1996, Reed et al. 2006; see also Dufty 1989), which is a classic life-history tradeoff. Impaired survival rate could result from various processes, for example from immune suppression (Folstad and Karter 1992) or an inhibition of molt by testosterone (e.g., Schleussner et al. 1985). Supporting the relationship between testosterone and fecundity traits found in intraspecific studies, several recent large-scale comparative analyses showed that the length of the breeding season was the factor that best explained interspecific variation in male testosterone concentrations during the breeding season (Goymann et al. 2004; Garamszegi et al. 2005, 2008). However, whether and in what way testosterone affects processes related to survival rate on an interspecific level is still unclear. Corticosterone has important regulatory functions on metabolism, behavior, and the immune system (Sapolsky et al. 2000). At baseline concentrations (in an undisturbed animal), corticosterone participates in regulating blood carbohydrate levels and energy stores (Sapolsky et al. 2000). Additionally, when an individual experiences acute adverse disturbances (e.g., a predator attack), corticosterone is released into the bloodstream at greatly increased concentrations. The function of such stress-induced corticosterone concentrations is to redirect behavioral and physiological processes away from other tasks (digestion, reproduction, etc.) and toward processes that aid in surviving the disturbance (increased locomotor activity, increased immune function, etc.; Wingfield et al. 1998, Sapolsky et al. 2000, Martin 2009). Indeed, increased corticosterone concentrations typically lead to increased locomotor activity (Breuner et al. 1998), energy mobilization (Sapolsky et al. 2000), and inhibition of reproduction (Wingfield and Sapolsky 2003). Acute increases in corticosterone also boost immune function (Dhabhar 2009) and have been suggested to enhance fitness in most but not all studies (Breuner et al. 2008). In light of these actions, corticosterone has been hypothesized to be involved in regulating the tradeoff between current versus future reproductive investment (e.g., Wingfield et al. 1995). Indeed, detailed intraspecific studies support a quantitative relationship between corticosterone concentrations (mostly stressinduced concentrations, but also baseline levels) and reproductive investment (e.g., in House Sparrows [Passer domesticus]; Lendvai et al. 2007, Lendvai and Chastel 2008). In interspecific studies, brood value (i.e., the value of the current brood in relation to future broods) has been found to explain a large part of the variation in stress-induced corticosterone concentrations (Wingfield et al. 1995, O'Reilly and Wingfield 2001, Holberton and Wingfield 2003) and in baseline corticosterone levels (Bókony et al. 2009). Until now, studies that explicitly link variations in testosterone and corticosterone concentrations among species to the pace of life in avian species have been lacking. Because procedures both in the field and laboratory can vary dramatically between studies and result in much unwanted variation, we conducted an original study on a set of temperate and tropical species to collect baseline corticosterone, stress-induced corticosterone, and testosterone concentrations in males during the breeding season. All samples were taken using identical procedures and were analyzed in the same laboratory (Hau et al., unpubl. data). Hormone concentrations were then related to key life-history traits such as fecundity and longevity. Following the physiology—life history concept (Ricklefs and Wikelski 2002), we predicted that species that adopt slow life histories (low reproductive rate, high survival rate) should reach higher stress-induced corticosterone concentrations if those function to increase processes related to survival and self-maintenance. Species with slow life histories should also reach lower testosterone concentrations during the breeding season, given that they typically show lower reproductive rates. Species on the fast end of the continuum were predicted to display opposite hormonal traits. As predicted, we found that stress-induced corticosterone concentrations were correlated with the survival rates of when we for (Hau et al., unpubl. data). testosterone concentrations were related to the reproductive of both corticosterone and testosterone concentrations with the slow—fast life-history which that these two hormones may be involved in mediating the pace of life in our data are together with the data they to the existence of an endocrine system that the regulation of life histories in avian species and in vertebrates in general. These new on the of these history and to in populations or species from (e.g., 2007, et al. 2009). birds of the tropical have been to have a more lower activity rates (Martin 1996, Wikelski and Ricklefs lower metabolic rates and and 1987, 1995, and et al. et al. and lower energy and Recently, tropical birds have also been to have a lower metabolic rate than temperate species et al. a that is not given the general relationship between and metabolic rate (Ricklefs et al. 1996). What is still known is the of energy by birds in the because field studies on the of tropical birds are to and to energy in the field are to birds can be in the for of the the et al. was by et al. for the first to all components of the energy of a tropical the The birds were much than they about per in and were for of the At the energy of males matched metabolic rate on laboratory studies in the However, in the were which that the birds may have in the this energy in a energy that was the value for a this size et al. 2009). has been found in other such as the and 2000), and et al. and Sparrows et al. it was that tropical birds may to this However, it is still why not lower and energy more at explanations for the of energy at metabolic levels at are that to be to or to processes at high levels the tropical For example, we found that more tropical species more energy on immune than or species et al. et al. unpubl. data). et al. we also the that tropical birds generally have a than Wikelski et al. unpubl. data). All tropical species show lower activity rates than as during the in tropical as compared with in Ricklefs These data support a general of in tropical birds compared with The immune system is an important component of and for with other to a to recognize a of in a and components during a The and of the immune system have been in and for and have more been into life-history of especially birds and 1996, et al. 2002). has been suggested that with high reproductive rates should in immune and 1996). of such has been with and related to the of the immune system and the of its in free-living have been et al. 2005, et al. and have a of that that immune are different among species of birds and that life-history can explain much of this is into and from continual investment in and whereas is to a in of new and in to a et al. the activity of blood from species of birds and found a with metabolic rate, which that species with a slower pace of life have a more immune et al. the relationship between life-history and in species of birds and found a relationship between and levels in adult which that longer of a more immune especially the is especially to The of the in to a with was in species of temperate and tropical birds unpubl. data). the of energy in the increased with size. differences in size were tropical species had higher levels of than temperate species that more had higher survival rates, and for a given survival rate temperate species had higher levels of than tropical can be from to offspring in the egg In species of small was a relationship between size and of which that larger species can more in the of offspring et al. 2009). and the of were may the value of with for of in species with a slower pace of The immune system is a of and it will to its detailed relationship with life histories. However, a has the immune of species with a slow pace of life have a higher level of but they are also to respond to a with greater of than those with a fast pace of variation among species in growth rates, which ornithologists have historically by species the rates the fitness of individuals and are by physiological and factors (Ricklefs 1969, Stearns et al. the as well as variation in has as The of and growth rate is larger species more both in and of the egg (Ricklefs and However, interesting variation the effects of size are and some of that variation is a function of are longer in tropical than in temperate birds (Ricklefs Recent has suggested that by tropical in to higher levels of nest predation (Ricklefs 1969, et al. 2000, Martin can the of (Martin and Martin 2007, and 2008). field studies suggested that behavioral of to of predation on or eggs However, a common that for effects of adult by eggs of temperate and tropical House found that the tropical eggs still longer to et al. 2008). that differences in nest not latitudinal differences in but that differences in how birds this variation across As with development, tropical also more than temperate Ricklefs found a slower rate of growth in of tropical birds as compared with temperate more species and a new that for with differences in and size at also found that tropical in more than temperate The same was for growth of it that tropical more than temperate it is interesting that are not longer in tropical that tropical birds at a size than temperate possible for is an influence of nest predation pressure species with higher rates of nest predation have offspring that (Ricklefs et al. 1998, and Martin 2002). of life-history is on variation in reproductive investment with to adult survival rate (i.e., the of future reproductive Stearns 1992, Roff 2002). Many comparative studies of avian life histories have on differences between tropical and temperate but it is important to have comparative data on survival rate as a function of of adult survival rates for tropical and temperate birds have from or studies (e.g., et al. studies have in the the and now and a for life histories in a demographic from the of breeding of a study may between tropical and temperate et al. 2000), the of these studies have both and about the of avian life histories at tropical on a of adult survival rates in and as well as in and of survival for tropical species available with studies by in the and with long-term studies in the et al. et al. and 2008). to higher survival rates in tropical than in temperate and this the more data and new or patterns (1) survival on higher in tropical than in temperate (2) the of survival and tropical species or survival (Ricklefs et al. Ricklefs and 2007). Thus, comparative on latitudinal variation in adult survival rates be on factors such as size and of adult survival have several for the evolution of life-history Because survival rates broadly between tropical and temperate adult survival cannot explain the more observed in the number of offspring per nesting et al. the that the that greater parental investment is with lower adult survival Martin et al. 2000a, Ghalambor and Martin is in the that survival the survival rate of offspring in the level of parental investment (Ricklefs of adult survival and the of survival that the level of parental investment (i.e., in should be in tropical and temperate in temperate not and it is a whether to in or offspring differences in brood size between tropical and temperate birds are to and food or other such as Ricklefs than parental investment. paper on latitudinal variation in clutch studies that have with the of why clutch size increases with latitude have the on avian lifehistory traits (Martin 1996, Ricklefs Ricklefs and Wikelski 2002). other of parental components of reproductive influence offspring and adult rates, food between breeding of parental nest nest and number of per studies, of tropical had been and most comparative studies focused on clutch size or not into in the analyses in Martin 1996). The from these studies were because differences in and of the study general patterns (Martin 1996). In the past 10 years, more studies and comparative analyses that for have been conducted and a toward of parental behavior other than clutch size has Recent comparative analyses have that tropical species tend to have parental et al. et al. lower nest (Martin 2002), longer (Martin et al. and greater egg (Martin et al. than temperate differences in rates and food are more to variation in nest predation (Martin et al. these recent how these different of parental are related to latitudinal variation in reproductive and parental strategies because have not been studies to comparative analyses of of per and nest (Ricklefs Ricklefs and understanding variation in reproductive requires understanding how to on a number of food For example, for the same rate, to offspring in an environment with food than in an environment food is readily how such environmental factors with latitude parental and are predicted to result in higher of survival reproduction are in tropical species (Ricklefs from the available of tropical species to have greater survival during the of on adult and or greater survival the first compared with many temperate species 2000, unpubl. data). this as more studies are it will suggest that reproductive should be or greater in tropical species compared with temperate species because of the high value of the offspring of tropical for the same level of reproductive tropical and species may different strategies of parental that offspring in tropical and offspring in temperate tradeoff between the of parental offspring and offspring and Stearns 1992) is by latitudinal variation in environmental For example, in species in which offspring is by offspring may increase parental fitness more than offspring in tropical for breeding and lower food during the breeding season, to populations on a Ricklefs et al. may investment in offspring to how environmental across latitudes, and more comparative analyses of parental are current that tropical birds offspring with parental and that variation in reproductive not explain variation in clutch size. analyses are important because they the between a range of adaptations that have with fitness and the of the tradeoffs and constraints in evolution and (Ricklefs 2000a). are for the comparative study of life-history and of diversification in because they have been well a range of and are more in some of behavior and demography than other of For such as and other which can be in the have many into the mechanisms that control of behavior and life histories (e.g., and 1998, and 2001, and is known about those in because birds can be in the we have the to how selection influence fitness of different life-history The of birds as for life-history includes the of studies and the of information about genetic factors that underlie life-history traits. However, new are our understanding of avian and show patterns of life-history variation, but it is not that they those of birds to the that general understanding will by from several For example, and exhibit more than birds and 1998, that the general are as in the of the of and most of studies of life-history variation in birds is the of how we given the of on the group the past years. many studies support the existence of tradeoffs, for example between reproductive and adult survival and 2002), the of such tradeoffs (e.g., how they which the of the have not been (Ricklefs 2000a). Many tropical species have and slow development, in of high nest predation (Ricklefs but has the of this (Ricklefs Martin et al. 2007). and the of food in patterns of reproductive rate in but food has not been a latitudinal for group of In of the importance of in population and the of in the of and 2000, and 2002), we have understanding of the of birds et al. et al. 2008). We tend to on what is and what is The of information on geographic in food and the of the with the the of explanations for reproductive rate, nest predation and related to adult survival 1993). to be about the diversification of avian life and it is an to be among the is whether is a single axis that the continuum of slow to fast life histories. important of variation will be revealed as we more about the that or of life-history for and in the field will new in our understanding of life-history The for example, of in the one can a once and a single blood to on the relationship between life-history and the immune system should be a future as new The multispecies comparative has been especially for patterns in life histories and for new Many of our have from studies that a small number of species because sufficient can be and because comparisons can be In most studies that have taken detailed at mechanisms have compared traits from one temperate and one tropical general of geographic patterns in life-history traits has been et al. 2008). Our nexus group has focused on one in temperate and one in The to from small of species and a of sites and then to patterns has been to The that nest predation and adult survival rates are generally greater in the are available data of in those rates across latitudes et al. et al. et al. 2000). Many data on other of life histories from a small number of and from a range of and life-history traits. Ornithologists should increase efforts to patterns in as well as in the to the of environmental gradients with life-history of sites between the temperate and tropical sites is more we can in life-history strategies and the pace of life In many of our from a number of in temperate and or in tropical and different strategies in species of or Ornithologists should multispecies comparisons and on new data that have been to historically but that may new of these data include of rates and and rates of to reproductive which will to in the key in demographic At the we still to the of between hormones and life-history the processes by which stress-induced corticosterone may be with survival rate and testosterone may be with The linkages of hormones with immune function also still to be evaluated in much to be advances in the of on field and laboratory and the of field data for comparative studies that this is an in the study of avian life histories. Our was by a in We the many and have been part of our nexus and have to our of avian life most of have or are in the We this paper to the of our