Exploring the role of life history traits and introduction effort in understanding invasion success in mammals: a case study of Barbary ground squirrels.

Primates show life history traits similar to those of cetaceans, such as small litter size, long gestation, long lactation, and long lifespan, in spite of striking contrasts in habitats, diet, mobility, and range size between them. Ecological factors (food and predation) may influence their life history traits in various ways, but social factors (social structure and reproductive strategies) may be more important for the life history of primates, in which both sexes live together even outside the breeding season. Group-living primates are classified into female-bonded species and female-dispersal species, based on the patterns of female dispersal after maturity. A comparison of life history parameters shows that female-dispersal species have a slower life history (gestation length, weaning age, age at first reproduction, and interbirth interval) than the female-bonded species, except for neonatal weight and weaning weight, which may be determined in relationship to female body weight. To elucidate factors promoting the slow life history, we focus on Atelinae and Hominidae (female-dispersal species) and examine their interspecific and intraspecific variation in social structure and male reproductive tactics in relationship to life history traits. Most Atelinae species form multimale and multifemale groups, and variation in their life history features may reflect relationships among males and their reproductive tactics. In howler monkeys, both males and females disperse, and infanticide by males may lead to a fast life history. In other Atelines, infanticide rarely occurs, although it has the effect of reducing interbirth interval. Forcible copulation by males occasionally occurs in spider monkeys. Variations in grouping among females reflecting their flexible foraging efforts according to distribution of high-quality foods may have some effects on the fast–slow continuum in the life history features of female Atelinae. Hominidae exhibit larger variations in life history features than Atelinae, probably because of their diverse social structure. Solitary nature and male reproductive tactics may have great influences on the life history of female great apes. Female orangutans, who usually live a solitary life, show the slowest life history. Maturing female orangutans need a longer time to establish their own home range and relationships with reproductive mates than female chimpanzees and gorillas, who transfer into other groups immediately after emigration. Female gorillas show the lowest age at first reproduction and the shortest interbirth interval. Intensive caretaking of the immature by male gorillas may facilitate early weaning, and infanticide by males may promote a prolonged bonding between a protector male and females to shorten the interbirth interval. Similar life history traits have been found in four long-term study sites of chimpanzees. Only females at Bossou show a fast life history, probably the result of high-quality foods and single male group composition under isolated conditions. The more frequent and stable association between females and males and more promiscuous mating in bonobos may facilitate the search for mating partners and lead to a shorter interbirth interval than chimpanzees. Frugivorous orangutans and chimpanzees may suffer more costs of female dispersal through decreased foraging efficiency than folivorous gorillas, and chimpanzees with fission–fusion grouping may suffer more social stress than gorillas in highly cohesive groups. Such differences may generally shape the fast–slow continuum of life history in female-dispersal primate species.KeywordsAge at first reproductionAtelinaeFemale-dispersal speciesHominidaeInterbirth intervalLife history

AimNon‐native fishes threaten native biodiversity worldwide. Life history traits have been used to predict the risk of establishment for non‐native fish in several regions of the world and parts of the United States, but not yet for Florida despite the elevated risk of establishment in the state due to many invasion pathways and favourable climate. Our goal was to identify which life history traits may be useful for predicting which non‐native freshwater fishes might successfully establish populations in Peninsular Florida.LocationPeninsular Florida, USA.MethodsWe conducted a factor analysis to evaluate 21 life history traits for 125 fishes in three different groups: native fishes, non‐native fish species currently established in Florida and introduced fishes that failed to establish in Florida. We also modelled overall life history traits of those fishes according to the triangular model by Winemiller and Rose to compare overall strategies among the three different groups and tested for significant trait differences between failed and established fishes.ResultsOur analyses of life history traits showed that successful species have a high investment in their offspring and tend to be larger bodied. Parental care was particularly important, with only one of the established species lacking parental care. Triangular life history model results showed that most successfully established species such as those in the family Cichlidae are equilibrium strategists with a high degree of parental care, low‐to‐intermediate fecundity and a larger maturation size.Main conclusionsUnderstanding the life history strategies and traits that aid in the prediction of non‐native fish invasiveness is key for effective risk assessment and management. Further analysis of these traits as predictors of establishment and invasion success is needed, and regional risk assessments of non‐native fishes will benefit from inclusion of several traits highlighted in this study.

Alien invaders

Through artificial selection and inbreeding, strains of laboratory mice have been developed that vary in the expression of a single or suite of desired traits valuable to biomedical research. In addition to the selected trait(s), these strains also display variation in pelage color, body size, physiology, and life history. This article exploits the broad phenotypic variation across lab mouse strains to evaluate the relationships between life history and metabolism. Life history variation tends to exist along a fast-slow continuum. There has been considerable interest in understanding the ecological and evolutionary factors underlying life history variation and the physiological and metabolic processes that support them. Yet it remains unclear how these key traits scale across hierarchical levels, as ambiguous empirical support has been garnered at the intraspecific level. Within-species investigations have been thwarted by methodological constraints and environmental factors that obscure the genetic architecture underlying the hypothesized functional integration of life history and metabolic traits. In this analysis, we used the publicly available Mouse Phenome Database by the Jackson Laboratory to investigate the relationships among life history traits (e.g., body size, reproduction, and life span) and metabolic traits (e.g., daily energy expenditure and insulin-like growth factor 1 concentration). Our findings revealed significant variation in reproductive characteristics across strains of mice as well as relationships among life history and metabolic traits. We found evidence of variation along the fast-slow life history continuum, though the direction of some relationships among these traits deviated from interspecific predictions laid out in previous literature. Furthermore, our results suggest that the strength of these relationships are strongest earlier in life.

Variation in life history (LH) traits along the fast-slow continuum (referred to as pace of life, POL) is thought to result from a trade-off between investments in current versus future reproduction. Originally developed for understanding variation in LH strategies at the among-population level, the POL theory has more recently been applied towards understanding variation in LH traits at the within-population level, and further extended to address the covariance of LH traits with additional behavioural and/or physiological traits, referred to as pace-of-life syndromes (POLS). The article by Reale et al. (Philos T Roy Soc B 365:4051–4063, 2010), which synthesized several earlier reviews and opinions on among-individual covariation between LH, behavioural, and physiological traits, and subsequent research testing POLS in a variety of species, have collectively been cited several hundreds of times—a trend that continues. These works have interdisciplinary impact, informing research in life history biology, behavioural and developmental biology, and the social sciences. In this paper, we review the existing theoretical POLS models that provide adaptive explanations for covariances between LH traits and additional behavioural and/or physiological traits while assuming a trade-off between current and future reproduction. We find that the set of relevant models is small. Moreover, models show that covariances between life history traits and behavioural or physiological traits can arise even in the absence of a current-future reproduction trade-off, implying that observing such covariances does not provide a strong indication regarding the process generating POLS. We discuss lessons learned from existing models of POLS, highlight key gaps in the modelling literature, and provide guidelines for better integration between theory and data.

(Re)appreciating the role of life history in eco‐evolutionary dynamics

Invasive species have the ability to modify their life-history traits in newly colonized areas, with positive shifts in specific life history traits under favourable environmental conditions. If such positive changes in their life history result in a comparably larger population growth rate, it may give them a competitive edge over native species, support faster range expansion and contribute to their invasion success. Within the present paper we hypothesized that the demographic flexibility represents an important contribution to the invasion success of exotic species, and that demographic flexibility patterns of invasive species differ from those in unsuccessful invaders. We tested this hypothesis by the use of elasticity analysis applied on simple age-structured population models of invasive fish species in the Danube River, as well as of non-native species that failed to establish or become invasive. Findings imply that the invasive fish species could have the ability to experience a more rapid population growth under favourable environmental conditions, especially those that sustain recruitment, while at the same time being more robust to changes in survival. The highest population elasticity among the assessed alien invasive species was detected in stone moroko (Pseudorasbora parva). The described approach has the potential to be used as an additional screening tool for invasive species. When combined with other invasion risk profiling methods, it can provide additional insight into characteristics of species invasions and in invasion potential of a species.

How do reproduction, parenting, and health cluster together? Exploring diverging destinies, life histories and weathering in two UK cohort studies.

The finding that passeriform birds introduced to the islands of Hawaii and Saint Helena were more likely to successfully invade when fewer other introduced species were present has been interpreted as strong support for the hypothesis that interspecific competition influences invasion success. I tested whether invasions were more likely to succeed when fewer species were present using the records of passeriform birds introduced to four acclimatization districts in New Zealand. I also tested whether introduction effort, measured as the number of introductions and the total number of birds released, could predict invasion outcomes, a result previously established for all birds introduced to New Zealand. I found patterns consistent with both competition and introduction effort as explanations for invasion success. However, data supporting the two explanations were confounded such that the greater success of invaders arriving when fewer other species were present could have been due to a causal relationship between invasion success and introduction effort. Hence, without data on introduction effort, previous studies may have overestimated the degree to which the number of potential competitors could independently explain invasion outcomes and may therefore have overstated the importance of competition in structuring introduced avian assemblages. Furthermore, I suggest that a second pattern in avian invasion success previously attributed to competition, the morphological overdispersion of successful invaders, could also arise as an artifact of variation in introduction effort.

Understanding why different life history strategies respond differently to changes in environmental variability is necessary to be able to predict eco-evolutionary population responses to change. Marine megafauna display unusual combinations of life history traits. For example, rays, sharks and turtles are all long-lived, characteristic of slow life histories. However, turtles also have very high reproduction rates and juvenile mortality, characteristic of fast life histories. Sharks and rays, in contrast, produce a few live-born young, which have low mortality rates, characteristic of slow life histories. This raises the question if marine megafaunal responses to environmental variability follow conventional life history patterns, including the pattern that fast life histories are more sensitive to environmental autocorrelation than slow life histories. To answer this question, we used a functional trait approach to quantify for different species of mobulid rays, cheloniid sea turtles and carcharhinid sharks – all inhabitants or visitors of (human-dominated) coastalscapes – how their life history, average size and log stochastic population growth rate, log(λs), respond to changes in environmental autocorrelation and in the frequency of favorable environmental conditions. The faster life histories were more sensitive to temporal frequency of favourable environmental conditions, but both faster and slower life histories were equally sensitive, although of opposite sign, to environmental autocorrelation. These patterns are atypical, likely following from the unusual life history traits that the megafauna display, as responses were linked to variation in mortality, growth and reproduction rates. Our findings signify the importance of understanding how life history traits and population responses to environmental change are linked. Such understanding is a basis for accurate predictions of marine megafauna population responses to environmental perturbations like (over)fishing, and to shifts in the autocorrelation of environmental variables, ultimately contributing toward bending the curve on marine biodiversity loss.

Ecological constraints, life history traits and the evolution of cooperative breeding

Studies of primate life history variation are constrained by the fact that all large-bodied extant primates are haplorhines. However, large-bodied strepsirrhines recently existed. If we can extract life history information from their skeletons, these species can contribute to our understanding of primate life history variation. This is particularly important in light of new critiques of the classic "fast-slow continuum" as a descriptor of variation in life history profiles across mammals in general. We use established dental histological methods to estimate gestation length and age at weaning for five extinct lemur species. On the basis of these estimates, we reconstruct minimum interbirth intervals and maximum reproductive rates. We utilize principal components analysis to create a multivariate "life history space" that captures the relationships among reproductive parameters and brain and body size in extinct and extant lemurs. Our data show that, whereas large-bodied extinct lemurs can be described as "slow" in some fashion, they also varied greatly in their life history profiles. Those with relatively large brains also weaned their offspring late and had long interbirth intervals. These were not the largest of extinct lemurs. Thus, we distinguish size-related life history variation from variation that linked more strongly to ecological factors. Because all lemur species larger than 10 kg, regardless of life history profile, succumbed to extinction after humans arrived in Madagascar, we argue that large body size increased the probability of extinction independently of reproductive rate. We also provide some evidence that, among lemurs, brain size predicts reproductive rate better than body size.

Amphibians have the least studied life histories among vertebrates, although they have unique and the most diverse life histories within this group. We compiled a new dataset on adult body mass and 16 other life history traits of 2069 amphibian species across three orders (1796 frogs, 236 salamanders, 37 caecilians). These traits characterise fecundity, offspring development from egg deposition to metamorphosis and adult life. We established allometric models on traits for all amphibians and each of the three orders to assess a potential scaling of traits to body mass and then checked whether allometric slopes were consistent with two different metabolic scaling exponents. Further, we examined a possible fast-slow continuum in all amphibians, as well as in each of the two orders frogs and salamanders by applying principal component analysis (PCA) to five traits. Our allometric models indicated a positive scaling to body mass for 11 traits across all amphibians, 12 in frogs, and 10 in salamanders, and for five out of eight traits analysed in caecilians. Allometric slopes on most traits characterising offspring development were not significant. All slopes did not support a three-quarter metabolic scaling exponent, whereas slopes on age at maturity and maximum longevity were consistent with an amphibian metabolic scaling exponent of 0.88. As in fishes, reptiles, birds, and mammals, the first axes of our PCAs indicated a body mass-dependent fast-slow continuum in amphibians. Amphibian species of slow life histories have larger body masses, later sexual maturities and longer lifespans and lay more and larger eggs than species of fast life histories, a pattern also known from reptiles. The second axes indicated a trade-off between egg size and number. As this trade-off was nearly independent of body mass, we hypothesise that amphibians have occupied a broad range of ecological niches without evolutionary changes in body mass.

AimBiological invasions threaten biodiversity globally. Large‐scale studies of non‐native plant species invasiveness typically focus on identifying ecological differences between naturalized and invasive species that account for their spread from sites of initial establishment (i.e., invasion success). However, invasive species differ widely in the magnitude of their impacts, suggesting the characteristics that favour invasion success might not necessarily predict the consequences of that invasion. Here we test whether those factors that increase the probability of plant species invasion also explain the severity of impacts.LocationChina.MethodsWe compiled a database of the invasiveness, biogeographic origins, life history traits, and introduction history for 538 non‐native plants in China and modelled differences in (a) naturalized and invasive species; (b) the spatial extent of invasion; and, (c) the severity of invasion impacts among successful invaders.ResultsInvasion success and the spatial extent of invasion shared similar influencing factors. However, these clearly differed from the predictors of severe invasion impacts. Unintentionally introduced non‐native plants with shorter life cycles and longer residence times were more likely to become invasive and to invade a larger area, while taller plants introduced from the Americas tended to have more severe impacts on the native ecosystems of China.Main ConclusionsThese results illustrate the different roles of introduction history, biogeographical origin and biological traits in determining the invasion success and spatial extent of invasion versus the severity of invasive species impacts. We suggest that factors associated with evolutionary adaptation and population expansion might determine invasion success and extent, while traits related to the relative competitive ability of invasive species determine the severity of impacts. Identifying specific characteristics of species that distinguish among successful invaders most likely to result in more severe impacts could help with planning more effective interventions.

Despite the diversity of mammalian life histories, persistent patterns of covariation have been identified, such as the 'fast-slow' axis of life-history covariation. Smaller species generally exhibit 'faster' life histories, developing and reproducing rapidly, but dying young. Hormonal mechanisms with pleiotropic effects may mediate such broad patterns of life-history variation. Insulin-like growth factor 1 (IGF-1) is one such mechanism because heightened IGF-1 activity is related to traits associated with faster life histories, such as increased growth and reproduction, but decreased lifespan. Using comparative methods, we show that among 41 mammalian species, increased plasma IGF-1 concentrations are associated with fast life histories and altricial reproductive patterns. Interspecific path analyses show that the effects of IGF-1 on these broad patterns of life-history variation are through its direct effects on some individual life-history traits (adult body size, growth rate, basal metabolic rate) and through its indirect effects on the remaining life-history traits. Our results suggest that the role of IGF-1 as a mechanism mediating life-history variation is conserved over the evolutionary time period defining mammalian diversification, that hormone-trait linkages can evolve as a unit, and that suites of life-history traits could be adjusted in response to selection through changes in plasma IGF-1.