First Fossil Evidence for the Advance of Replacement Teeth Coupled with Life History Evolution along an Anagenetic Mammalian Lineage

In mammals that grow up more slowly and live longer, replacement teeth tend to appear earlier in sequence than in fast growing mammals. This trend, known as ‘Schultz''s Rule’, is a useful tool for inferring life histories of fossil taxa. Deviations from this rule, however, suggest that in addition to the pace of life history, ecological factors may also drive dental ontogeny. Myotragus balearicus is an extinct insular caprine that has been proved to be an excellent test case to correlate morphological traits with life history. Here we show that Myotragus balearicus exhibits a slow signature of dental eruption sequence that is in agreement with the exceptionally slow life history of this species, thus conforming to ‘Schultz''s Rule’. However, our results also show an acceleration of the absolute pace of development of the permanent incisors in relation to that of the posterior teeth. The rodent-like incisors of Myotragus balearicus erupted early not only in relative but also in absolute terms (chronological age), suggesting that feeding characteristics also plays an important role in dental ontogeny. This is in agreement with ecological hypotheses based on primates. Our study documents a decoupling of the pace of development of teeth in mammals that is triggered by different selection pressures on dental ontogeny. Moreover, we show that Myotragus kopperi from the early Pleistocene (a direct ancestor of the late Pleistocene-Holocene M. balearicus) follows the pattern of first incisor replacement known in living bovids. Hence, the advance in the eruption sequence of the first incisors occurs along the Myotragus evolutionary lineage over a period of about 2.5 Myr. To our knowledge, this is the first fossil evidence of an advance of the emergence of the permanent first incisor along an anagenetic mammalian lineage.     

Indications for a dietary change in the extinct Bovid genus Myotragus (Plio-Holocene,Mallorca, Spain)

Evolution in isolated island has shaped a variety of endemic taxa with outstanding characteristics. Amongst them is the extinct bovid genus Myotragus, endemic to Mallorca and Menorca Island, for which six succeeding species have been described: M. palomboi, M. pepgonellae, M. antiquus, M. kopperi, M. batei and M. balearicus. Myotragus has developed special cranial and post-cranial adaptations to meet the specific ecological demands of its insular habitat, like progressive dwarfing and fused limb elements. During its evolution, the dentition of Myotragus underwent subsequent changes: firstly a reduction in the number of teeth, and secondly an increase in hypsodonty. The ecological conditions inducing this dental evolution, especially Myotragus’ diet, remain unknown. In this study, methods of 3D-dental topometry, enamel surface texture analysis according to ISO/FDIS 25178-2, and Scale-Sensitive Fractal Analysis (SSFA) are applied in order to infer palaeodiets of M. pepgonellae, M. kopperi, M. batei and M. balearicus, and to test the hypothesis that a dietary change may have occurred in the Myotragus lineage which relates to gradual morphological changes on upper second molars. We detect changes in the enamel/dentin ratio, enamel ridge length and enamel surface area within the lineage. Furthermore, Myotragus balearicus has enamel surface texture characteristics also present in extant browsing ungulates, while the three antecedent Myotragus species show an enamel surface texture signal similar to extant grazers. These results suggest a dietary change and are interpreted as a successive adaptation to limited resources in an isolated, insular environment. They can either be a consequence of a change in plant community structure or a successive expansion of Myotragus’ dietary range due to increased intraspecific competition.     

Dietary divergence in space and time – Lessons from the dwarf-goat Myotragus balearicus (Pleisto-Holocene,Mallorca, Spain)

Newly colonised, isolated habitats, like islands, provide diverse niches to be filled and are prone to facilitate ecological separation which might lead to an adaptive radiation. Examples of such radiations can be found in the Mediterranean for the genera Candiacervus (Crete), Nesogoral (Sardinia) and Hoplitomeryx (Gargano). A different strategy to cope with limited resources on islands is generalism. We test whether populations of the endemic bovid Myotragus balearicus from two sites and Pleistocene as well as Holocene levels on Mallorca island displays ecological separation indicated by diet, or whether the species shifted its dietary trait towards generalism. We expect to find either: (1) dietary divergence in space and time (between sites and stratigraphic levels), which would indicate niche partitioning and/or a shift in dietary traits due to environmental influences; or (2) dietary congruence in a less specialised, generalistic dietary strategy in space and time which would indicate a flexible trait to cope with instable resource availability. We compare individuals from a fossil assemblage at a northern site and one assemblage from the eastern coast in terms of their dietary traits. Traits are reconstructed using dental dietary proxies, complementary in time scale and resolution. (1) 3D-dental topometry and (2) enamel surface texture analysis. Data suggest that individuals from both assemblages of M. balearicus behaved as variable browse dominated intermediate feeders. We thus conclude that the observed variability relates to a shift towards generalism as a subsistence strategy. We consider hypsodonty the pre-adaptation for this life style that enabled M. balearicus to exploit almost any food source in its energetically restricted island habitat.     

Phenotypic selection and covariation in the life‐history traits of elephant seals: heavier offspring gain a double selective advantage

Early developmental conditions contribute to individual heterogeneity of both phenotypic traits and fitness components, ultimately affecting population dynamics. Although the demographic consequences of ontogenic growth are best quantified using an integrated measure of fitness, most analyses to date have instead studied individual fitness components in isolation. Here, we estimated phenotypic selection on weaning mass in female southern elephant seals Mirounga leonina by analyzing individual‐based data collected between 1986 and 2016 with capture–recapture and matrix projection models. In support of a hypothesis predicting a gradual decrease of weaning mass effects with time since weaning (the replacement hypothesis), we found that the estimated effects of weaning mass on future survival and recruitment probability was of intermediate duration (rather than transient or permanent). Heavier female offspring had improved odds of survival in early life and a higher probability to recruit at an early age. The positive link between weaning mass and recruitment age is noteworthy, considering that pre‐recruitment mortality already imposed a strong selective filter on the population, leaving only the most ‘robust’ individuals to reproduce. The selection gradient on asymptotic population growth rate, a measure of mean absolute fitness, was weaker than selection on first‐year survival and recruitment probabilities. Weaker selection on mean fitness occurs because weaning mass has little impact on adult survival, the fitness component to which the population growth of long‐lived species is most sensitive. These results highlight the need to interpret individual variation in phenotypic traits in a context that considers the demographic pathways between the trait and an inclusive proxy of individual fitness. Although variation in weaning mass do not translate to permanent survival differences among individuals in adulthood, it explains heterogeneity and positive covariation between survival and breeding in early life, which contribute to between‐individual variation in fitness.     

Where to Dig for Fossils: Combining Climate-Envelope,Taphonomy and Discovery Models

Fossils represent invaluable data to reconstruct the past history of life, yet fossil-rich sites are often rare and difficult to find. The traditional fossil-hunting approach focuses on small areas and has not yet taken advantage of modelling techniques commonly used in ecology to account for an organism’s past distributions. We propose a new method to assist finding fossils at continental scales based on modelling the past distribution of species, the geological suitability of fossil preservation and the likelihood of fossil discovery in the field, and apply it to several genera of Australian megafauna that went extinct in the Late Quaternary. Our models predicted higher fossil potentials for independent sites than for randomly selected locations (mean Kolmogorov-Smirnov statistic = 0.66). We demonstrate the utility of accounting for the distribution history of fossil taxa when trying to find the most suitable areas to look for fossils. For some genera, the probability of finding fossils based on simple climate-envelope models was higher than the probability based on models incorporating current conditions associated with fossil preservation and discovery as predictors. However, combining the outputs from climate-envelope, preservation, and discovery models resulted in the most accurate predictions of potential fossil sites at a continental scale. We proposed potential areas to discover new fossils of Diprotodon, Zygomaturus, Protemnodon, Thylacoleo, and Genyornis, and provide guidelines on how to apply our approach to assist fossil hunting in other continents and geological settings.     

Climate and mammalian life histories

Mammals display considerable geographical variation in life history traits. To understand how climatic factors might influence this variation, we analysed the relationship between life history traits – adult body size, litter size, number of litters per year, gestation length, neonate body mass, weaning age and age at sexual maturity – and several environmental variables quantifying the seasonality and predictability of temperature and precipitation across the distribution range of five terrestrial mammal groups. Environmental factors correlated strongly with each other; therefore, we used principal components analysis to obtain orthogonal climatic predictors that could be used in multivariate models. We found that in bats, primates and even‐toed ungulates adult body size tends to be larger in species inhabiting cold, dry, seasonal environments, whereas in carnivores and rodents a smaller body size is characteristic of warm, dry environments, suggesting that low food availability might limit adult size. Species inhabiting cold, dry, seasonal habitats have fewer, larger litters and shorter gestation periods; however, annual fecundity in these species is not higher, implying that the large litter size of mammals living at high latitudes is probably a consequence of time constraints imposed by strong seasonality. On the other hand, the number of litters per year and annual fecundity were greater in species inhabiting environments with higher seasonality in precipitation. Lastly, we found little evidence for specific effects of environmental variability. Our results highlight the complex effects of environmental factors in the evolution of life history traits in mammals. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 719–736.     

Selection on QTL and complex traits in complex environments

Understanding genetic variation for complex traits in heterogeneous environments is a fundamental problem in biology. In this issue of Molecular Ecology, Fournier‐Level et al. ( 2013 ) analyse quantitative trait loci (QTL) influencing ecologically important phenotypes in mapping populations of Arabidopsis thaliana grown in four habitats across its native European range. They used causal modelling to quantify the selective consequences of life history and morphological traits and QTL on components of fitness. They found phenology QTL colocalizing with known flowering time genes as well as novel loci. Most QTL influenced fitness via life history and size traits, rather than QTL having direct effects on fitness. Comparison of phenotypes among environments found no evidence for genetic trade‐offs for phenology or growth traits, but genetic trade‐offs for fitness resulted because flowering time had opposite fitness effects in different environments. These changes in QTL effects and selective consequences may maintain genetic variation among populations.     

A test of the thermal coadaptation hypothesis with ultimate measures of fitness in flour beetles

Whole-organism performance of ectotherms depends on body temperature, which is tightly linked to environmental temperatures. Individuals attempting to optimize fitness must thus select appropriate temperatures. The thermal coadaptation hypothesis posits that T_o for traits closely linked to fitness should match temperatures selected by a species (T_set) and should coevolve with T_set. T_o may mismatch T_set if the thermal reaction norm for fitness is asymmetric. In this study, we examined six traits related to fitness in red and in confused flour beetles (Tribolium castaneum and T. confusum, respectively), including longevity, lifetime reproductive success, reproductive rate, and development time at four temperatures between 23 and 32 °C. For reproductive traits, T_o matched T_set whereas for longevity T_o was lower than T_set. Tribolium species have a strongly r-selected life history strategy, therefore reproductive traits are likely more tightly linked to fitness than longevity due to high predation rates at early life stages. We therefore provide support for the thermal coadaptation hypothesis for reproductive traits that are tightly linked to fitness. Our results highlight the importance of knowing the relationships of traits to fitness when studying thermal physiology.     

Adaptations and phenotypic plasticity in developmental traits of Marshallagia marshalli

Despite the economic, social and ecological importance of the ostertagiine abomasal nematode Marshallagia marshalli, little is known about its life history traits and its adaptations to cope with environmental extremes. Conserved species-specific traits can act as exaptations that may enhance parasite fitness in changing environments. Using a series of experiments, we revealed several unique adaptations of the free-living stages of M. marshalli that differ from other ostertagiines. Eggs were isolated from the feces of bighorn sheep (Ovis canadensis) from the Canadian Rocky Mountains and were cultured at different temperatures and with different media. Hatching occurred primarily as L1s in an advanced stage of development, morphologically very similar to a L2. When cultured at 20 °C, however, 2.86% of eggs hatched as L3, with this phenomenon being significantly more common at higher temperatures, peaking at 30 °C with 28.95% of eggs hatching as L3s. After hatching, free-living larvae of M. marshalli did not feed nor grow as they matured from L1 to infective L3. These life history traits seem to be adaptations to cope with the extreme environmental conditions that Marshallagia faces across its extensive latitudinal distribution in North America and Eurasia. In order to refine the predictions of parasite dynamics under scenarios of a changing climate, basic life history traits and temperature-dependent phenotypic behaviour should be incorporated into models for parasite biology.     

Contrasting patterns of sexually selected traits in Mediterranean and continental populations of European mouflon

The expression of sexually selected traits in highly dimorphic ungulates may be influenced by environmental quality. Variations in habitat conditions can impose different constraints on the allocation of energy resources to male life‐history traits, and possibly alter the female preferences for specific features. Here, we compared the horn growth patterns in male European mouflon Ovis aries musimon living in different habitats (Mediterranean vs. continental) but sharing a common genetic origin. We hypothesized that the expression of sexually selected traits such as horn development should be promoted in more favorable habitat conditions (i.e., Mediterranean). Using linear mixed models on data retrieved from individuals harvested under the same hunting regime, we found longer horns and greater individual variance in horn segment length in the Mediterranean population than in the continental one. Furthermore, Mediterranean rams showed no evidence of compensatory horn growth, as opposed to the continental rams. Unexpectedly, horn base circumference was greater in the continental habitat than in the Mediterranean one. The overall results suggest different patterns of investment in horns in the two populations, with seemingly stronger pressure and consequences of sexual selection on mouflon rams living in more favorable environments. Although the role of hunters' selectivity cannot be excluded a priori, our data suggest that the differences in the expression of sexually selected traits in our study populations may be influenced by environmental conditions. Because sexual selection can impose substantial fitness costs on individuals, further investigations on the trade‐offs between reproduction and survival would improve our understanding of the dynamics of mouflon populations living in different environmental conditions.     

Exposure to light enhances pre-adult fitness in two dark-dwelling sympatric species of ants

Background  

In insects, circadian clocks play a key role in enhancing fitness by regulating life history traits such as developmental time and adult lifespan. These clocks use environmental light/dark (LD) cycles to fine-tune a wide range of behavioral and physiological processes. To study the effect of environmental LD conditions on pre-adult fitness components, we used two dark-dwelling sympatric species of ants (the night active Camponotus compressus and the day active Camponotus paria), which normally develop underground and have fairly long pre-adult developmental time.     

Co‐inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region

Co‐inheritance in life‐history traits may result in unpredictable evolutionary trajectories if not accounted for in life‐history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life‐history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that these two traits are co‐inherited around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8–3.5 90% CI) times higher for fish with the early‐maturing vgll3 genotype (EE) compared to fish with the late‐maturing genotype (LL). The L allele was dominant in individuals remaining only one year at sea before maturation, but the dominance was reversed, with the E allele being dominant in individuals maturing after two or more years at sea. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first‐time spawners, across all age groups, whereas this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life‐history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments.     

The genetics of adaptation to novel environments: selection on germination timing in Arabidopsis thaliana

When studying selection during adaptation to novel environments, researchers have often paid little attention to an organism’s earliest developmental stages. Despite this lack of attention, early life history traits may be under strong selection during colonization, as the expression of adaptive phenotypes at later points is contingent upon early survival. Moreover, the timing of early developmental transitions can constrain the timing of later transitions, with potentially large effects on fitness. In this issue, Huang et al. (2010) underscore the importance of early life history traits in the adaptation of Arabidopsis thaliana to old‐field sites in North America. Using a new population of mapped recombinant inbred lines, the authors examined germination timing and total lifetime fitness of A. thaliana while varying site latitude, dispersal season, and maternal photoperiod. Huang et al. (2010) discovered several Quantitative Trait Loci (QTL) with large effects on fitness that colocalized with QTL for field germination timing and seed dormancy—demonstrating that fitness is genetically associated with these early life history traits, and that these loci are likely under strong selection during adaptation to novel environments. In the epistatic interactions of some loci, recombinant genotypes outperformed parental genotypes, supporting the potentially adaptive role of recombination. This study provides elegant evidence that traits expressed early in an organism’s development can play an important role during adaptive evolution.     

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment‐specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2‐5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.     

Life history of an invasive and unexploited population of Nile tilapia (Oreochromis niloticus) and geographical variation across its native and non-native ranges

Although the life history traits of Nile tilapia, Oreochromis niloticus have been studied since the early 20^th century, the potential range of life history parameters in unexploited populations and geographical variability in life history traits are still poorly understood. We explored life history traits (age composition, growth rate, mortality, size, and age at maturity) of an invasive and unexploited population in the Tabaru River, Yonaguni-jima Island, southwestern Japan, through comparisons with exploited populations across the species’ global distribution. Analysis of sectioned otoliths from 307 fish revealed that growth and maximum age were sexually dimorphic (females growing less but having greater longevity). Large-scale comparisons with exploited populations revealed that the unexploited Tabaru River population had a greater life span than exploited populations in other regions, but the growth rate was in the middle of the range of observed values. Although a high variation in life history parameters was observed among populations (L _∞, K, maximum age), we found no significant variation in life history traits by latitude or between African and non-African populations. Such a combination of long life span and high variability in life history traits in response to environmental and fishing pressures may aid the success of non-native Nile tilapia in various environments.     

Reproductive and post‐reproductive life history of wild‐caught Drosophila melanogaster under laboratory conditions

The life history of the fruit fly (Drosophila melanogaster) is well understood, but fitness components are rarely measured by following single individuals over their lifetime, thereby limiting insights into lifetime reproductive success, reproductive senescence and post‐reproductive lifespan. Moreover, most studies have examined long‐established laboratory strains rather than freshly caught individuals and may thus be confounded by adaptation to laboratory culture, inbreeding or mutation accumulation. Here, we have followed the life histories of individual females from three recently caught, non‐laboratory‐adapted wild populations of D. melanogaster. Populations varied in a number of life‐history traits, including ovariole number, fecundity, hatchability and lifespan. To describe individual patterns of age‐specific fecundity, we developed a new model that allowed us to distinguish four phases during a female's life: a phase of reproductive maturation, followed by a period of linear and then exponential decline in fecundity and, finally, a post‐ovipository period. Individual females exhibited clear‐cut fecundity peaks, which contrasts with previous analyses, and post‐peak levels of fecundity declined independently of how long females lived. Notably, females had a pronounced post‐reproductive lifespan, which on average made up 40% of total lifespan. Post‐reproductive lifespan did not differ among populations and was not correlated with reproductive fitness components, supporting the hypothesis that this period is a highly variable, random ‘add‐on’ at the end of reproductive life rather than a correlate of selection on reproductive fitness. Most life‐history traits were positively correlated, a pattern that might be due to genotype by environment interactions when wild flies are brought into a novel laboratory environment but that is unlikely explained by inbreeding or positive mutational covariance caused by mutation accumulation.     

Contrasting life history strategies of sympatric Arctic charr morphs, Salvelinus alpinus

In polymorphic populations morphs usually diverge in morphology, ecology and life history, which is most likely driven by adaptations to different environments or resources. Sympatric morphs may develop differences in several life history traits to be able to maximize fitness in alternative niches and habitats. Here, the contrasting life history traits of three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs in a deep and oligotrophic lake in sub-arctic Norway are addressed. The charr morphs differ in spawning habitat and trophic niche. One is a littoral spawning morph that feeds on benthic invertebrates and zooplankton in the littoral and pelagic zones (referred to as the LO-morph), and two other are profundal spawning morphs that either utilize profundal soft bottom benthos as food resource (the PB-morph) or are piscivorous (the PP-morph). The LO-morph typically had intermediate life-history traits relative to the two profundal morphs that had highly contrasting life history traits, especially in growth and age and size of maturity. The PB-morph matured at a young age (～3 years) and at a small body size (～8.5 cm), thereby increasing their fitness by investing in reproduction early in life, which results in a short generation time and decreased probability of being predated before first reproduction. The PP-morph on the other hand, matured at an old age (～9.2 years) and a large body size (～26 cm), thereby increasing their fitness by investing in somatic growth to enhance initial fecundity, and also to reach a large body size profitable for piscivory. The different trade-off regime between the PP- and PB-morphs seems to be caused by adaptation to alternative trophic niches, and appears to be an important factor for the co-occurrence of the two sister-morphs in the profundal zone.     

Evolutionary potential of morphological traits across different life‐history stages

Despite accumulating examples of selection acting on heritable traits in the wild, predicted evolutionary responses are often different from observed phenotypic trends. Various explanations have been suggested for these mismatches. These include within‐individual changes across lifespan that can create important variation in genetic architecture of traits and selection acting on them, but also potential problems with the methodological approach used to predict evolutionary responses of traits. Here, we used an 8‐year data set on tree swallow (Tachycineta bicolor) to first assess the effects of differences among three nestling life‐history stages on the genetic (co)variances of two morphological traits (body mass and primary feather length) and the selection acting on them over three generations. We then estimated the evolutionary potential of these traits by predicting their evolutionary responses using the breeder's equation and the secondary theorem of selection approaches. Our results showed variation in strength and direction of selection and slight changes in trait variance across ages. Predicted evolutionary responses differed importantly between both approaches for half of the trait–age combinations we studied, suggesting the presence of environmentally induced correlations between focal traits and fitness possibly biasing breeder's equation predictions. Our results emphasize that predictions of evolutionary potential for morphological traits are likely to be highly variable, both in strength and direction, depending on the life stage and method used, thus mitigating our capacity to predict adaptation and persistence of wild populations.     

Effects of Harsh and Unpredictable Environments in Adolescence on Development of Life History Strategies

The National Longitudinal Study of Adolescent Health data were used to test predictions from life history theory. We hypothesized that (1) in young adulthood an emerging life history strategy would exist as a common factor underlying many life history traits (e.g., health, relationship stability, economic success), (2) both environmental harshness and unpredictability would account for unique variance in expression of adolescent and young adult life history strategies, and (3) adolescent life history traits would predict young adult life history strategy. These predictions were supported. The current findings suggest that the environmental parameters of harshness and unpredictability have concurrent effects on life history development in adolescence, as well as longitudinal effects into young adulthood. In addition, life history traits appear to be stable across developmental time from adolescence into young adulthood.

The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history.

Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness.

Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.