Female post-reproductive lifespan: a general mammalian trait

Traditional explanations for the evolution of menopause and post-reproductive lifespan in human females have been based on the benefits of maternal or grand-maternal care outweighing the cost of lost reproduction. These explanations assume an evolutionary origin of menopause since human divergence with the most recent common ancestor. In this study, I conduct a literature survey of studies of 42 mammal species from eight orders, showing that post-reproductive lifespan appears to be widespread among mammals. I then propose an alternative to traditional hypotheses: following accepted theories of trade-offs and senescence, I suggest that the cost of extending reproductive lifespan might be relatively high in female mammals. Somatic and reproductive senescence appear to follow separate trajectories, so it is not surprising that the two processes should occur on different schedules. The timing of each process is probably determined by maximization of reproductive performance and survival early in adulthood, with consequent trajectories resulting in a post-reproductive lifespan. The early end of reproduction relative to lifespan may be due to the cost of production and/or maintenance of oocytes, which decline exponentially over time. Oocyte number below a threshold may trigger an end to normal hormonal cycling.     

Patterns of philopatry and longevity contribute to the evolution of post-reproductive lifespan in mammals

While menopause has long been known as a characteristic trait of human reproduction, evidence for post-reproductive lifespan (PRLS) has recently been found in other mammals. Adaptive and non-adaptive hypotheses have been proposed to explain the evolution of PRLS, but formal tests of these are rare. We use a phylogenetic approach to evaluate hypotheses for the evolution of PRLS among mammals. In contrast to theoretical models predicting that PRLS may be promoted by male philopatry (which increases relatedness between a female and her group in old age), we find little evidence that male philopatry led to the evolution of a post-reproductive period. However, the proportion of life spent post-reproductive was related to lifespan and patterns of philopatry, suggesting that the duration of PRLS may be impacted by both non-adaptive and adaptive processes. Finally, the proportion of females experiencing PRLS was higher in species with male philopaty and larger groups, in accordance with adaptive models of PRLS. We suggest that the origin of PRLS primarily follows the non-adaptive ‘mismatch’ scenario, but that patterns of philopatry may subsequently confer adaptive benefits of late-life helping.     

Postreproductive lifespans are rare in mammals

A species has a post‐reproductive stage if, like humans, a female entering the adult population can expect to live a substantial proportion of their life after their last reproductive event. However, it is conceptually and statistically challenging to distinguish these true post‐reproductive stages from the usual processes of senescence, which can result in females occasionally surviving past their last reproductive event. Hence, despite considerable interest, the taxonomic prevalence of post‐reproductive stages remains unclear and debated. In this study we use life tables constructed from published data on wild populations of mammals, and statistical measures of post‐reproductive lifespans, to distinguish true post‐reproductive stages from artefacts of senescence and demography in 52 species. We find post‐reproductive stages are rare in mammals and are limited to humans and a few species of toothed whales. By resolving this long‐standing debate, we hope to provide clarity for researchers in the field of evolutionary biology and a solid foundation for further studies investigating the evolution and adaptive significance of this unusual life history trait.     

The human post‐fertile lifespan in comparative evolutionary context

There persist two widely held but mutually inconsistent views on the evolution of post‐fertile lifespan of human females. The first, prevalent within anthropology, sees post‐fertile lifespan (PFLS) in the light of adaptive processes, focusing on the social and economic habits of humans that selected for a lengthy PFLS. 1 - 3 This view rests on the assumption that human PFLS is distinct from that of other species, and focuses on quantifying the selective causes and consequences of that difference. The second view, prevalent within gerontology and comparative biology, emphasizes that PFLS is a phylogenetically widespread trait 4 - 6 or that human PFLS is predictable based on life‐history allometries. 7 In this view, human PFLS is part of a broad cross‐species pattern and its genesis cannot, therefore, rely on human‐specific traits. Those who advocate the second view have questioned the “special pleading” for human specific explanations of PFLS, 4 and have argued that human PFLS is quantitatively greater but not qualitatively different than PFLS in many other animals. 5 , 8 Papers asking whether human PFLS is explained by the importance of mothers more than grandmothers, whether paternal or maternal grandparents have more of an effect on child survival, or who is providing the excess calories are associated with the first view that assumes the need to explain the existence of human PFLS on the basis of a uniquely human socioecology. Anthropologists largely see human PFLS as derived, while comparative gerontologists point to evidence that it is one instance of a ubiquitous cross‐species pattern. The two groups generally occupy non‐overlapping research circles, in terms of conferences and journals, and therefore interact little enough to largely avoid the need to reconcile their views, allowing the persistence of misconceptions in each field. Our goal is to identify and address the most important of these misconceptions and thereby make clear that both of these seemingly incongruent views contain valid points. We argue that two distinct but related traits have been lumped together under the same concept of “post‐reproductive lifespan,” one (post‐fertile viability) that is tremendously widespread and another (a post‐fertile life stage) that is derived to hominins, and that the differences and connections between these two traits are necessary for understanding human life‐history evolution.     

Hybrid crosses and the genetic basis of interspecific divergence in lifespan in Pristionchus nematodes

Characterizing the genetic basis of among‐species variation in lifespan is a major goal of evolutionary gerontology research, but the very feature that defines separate species – the inability to interbreed – makes achieving this goal impractical, if not impossible, for most taxa. Pristionchus nematodes provide an intriguing system for tackling this problem, as female lifespan varies among species that can be crossed to form viable (although infertile) hybrids. By conducting reciprocal crosses among three species – two dioecious (long‐lived Pristionchus exspectatus and short‐lived Pristionchus arcanus) and one androdioecious (short‐lived Pristionchus pacificus) – we found that female lifespan was long for all hybrids, consistent with the hypothesis that the relatively short lifespans seen for P. pacificus hermaphrodites and P. arcanus females are caused by independent, recessive alleles that are masked in hybrid genomes. Cross‐direction had a small effect on survivorship for crosses involving P. exspectatus, indicating that nuclear–mitochondrial interactions may also influence Pristionchus longevity. Our findings suggest that long lifespan in P. exspectatus reflects the realization of an ancestral potential for extended longevity in the P. pacificus species complex. This work demonstrates the utility of interspecific hybrids for ageing research and provides a foundation for future work on the genetic architecture of interspecific lifespan variation.     

Sexual selection did not contribute to the evolution of male lifespan under curtailed age at reproduction in a seed beetle

1. Sexual selection is a powerful evolutionary force that is hypothesised to play an important role in the evolution of lifespan. Here we test for the potential contribution of sexual selection to the rapid evolution of male lifespan in replicated laboratory populations of the seed beetle, Callosobruchus maculatus. 2. For 35 generations, newly hatched virgin male beetles from eight different populations were allowed to mate for 24 h and then discarded. Sexual selection was removed in half of these populations by enforcing random monogamy. 3. Classic theory predicts that because of sexual competition, males from sexually selected lines would have higher age‐specific mortality rates and shorter lifespan than males from monogamous lines. 4. Alternatively, condition‐dependent sexual selection may also favour genes that have positive pleiotropic effects on lifespan and ageing. 5. Males from all eight populations evolved shorter lifespans compared with the source population. However, there was no difference in lifespan between males from populations with or without sexual selection. Thus, sexual selection did not contribute to the evolution of male lifespan despite the fact that such evolution did occur in our study populations.     

利用形态学及mtDNA基因分子鉴定长须鲸和大村鲸

大型鲸类死亡个体,往往因腐烂程度较高或外部形态损坏,很难鉴定物种。2018年11月和2019年1月在江苏南通和浙江宁波各发现一头死亡须鲸。本文仔细辩别了两头须鲸的形态学特征,又应用分子生物学技术,分别得到903 bp和972 bp mtDNA控制区序列,以及467 bp和438 bp Cyt b序列。经GeneBank 序列比对,南通样本与长须鲸相似度最高,达99%~100%;宁波样本与大村鲸相似度最高,达97%~99%。通过MEGA 7.0软件的最大似然法（ML）构建的系统发育树与Blast结果一致。综上,南通死亡须鲸鉴定为长须鲸,宁波死亡须鲸鉴定为大村鲸。同时,由于这两个物种在中国的分布信息比较缺乏,本研究证实了长须鲸在江苏省南通市及大村鲸在浙江省宁波市象山县的新分布。     

Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo-identification data with high-resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource- and/or mate-defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until approximately 15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.     

Telomere length is repeatable,shortens with age and reproductive success,and predicts remaining lifespan in a long‐lived seabird

Telomeres are protective caps at the end of chromosomes, and their length is positively correlated with individual health and lifespan across taxa. Longitudinal studies have provided mixed results regarding the within‐individual repeatability of telomere length. While some studies suggest telomere length to be highly dynamic and sensitive to resource‐demanding or stressful conditions, others suggest that between‐individual differences are mostly present from birth and relatively little affected by the later environment. This dichotomy could arise from differences between species, but also from methodological issues. In our study, we used the highly reliable Terminal Restriction Fragment analysis method to measure telomeres over a 10‐year period in adults of a long‐lived seabird, the common tern (Sterna hirundo). Telomeres shortened with age within individuals. The individual repeatability of age‐dependent telomere length was high (>0.53), and independent of the measurement interval (i.e., one vs. six years). A small (R² = .01), but significant part of the between‐individual variation in telomere length was, however, explained by the number of fledglings produced in the previous year, while reproduction in years prior to the previous year had no effect. We confirmed that age‐dependent telomere length predicted an individual's remaining lifespan. Overall, our study suggests that the majority of between‐individual variation in adult telomere length is consistent across adult life, and that a smaller part of the variation can be explained by dynamic factors, such as reproduction.     

Diel variation in beaked whale diving behavior

We investigate diel variation in beaked whale diving behavior using data from time–depth recorders deployed on six Blainville's ( Mesoplodon densirostris) (255 h) and two Cuvier's ( Ziphius cavirostris ) (34 h) beaked whales. Deep foraging dives (>800 m) occurred at similar rates during the day and night for Blainville's beaked whales, and there were no significant diel differences in ascent rates, descent rates, or mean or maximum depths or durations for deep dives. Dive to mid-water depths (100–600 m) occurred significantly more often during the day (mean = 1.59 h⁻¹) than at night (mean = 0.26 h⁻¹). Series of progressively shallower "bounce" dives were only documented to follow the deep, long dives made during the day; at night whales spent more time in shallow (<100 m) depths. Significantly slower ascent rates than descent rates were found following deep foraging dives both during the day and night. Similar patterns were found for the Cuvier's beaked whales. Our results suggest that so-called "bounce" dives do not serve a physiological function, although the slow ascents may. This diel variation in behavior suggests that beaked whales may spend less time in surface waters during the day to avoid near-surface, visually oriented predators such as large sharks or killer whales ( Orcinus orca ).     

Sexual dimorphism in the human post-reproductive life-span: Possible causes

The fact that human females exhibit a post-reproductive life-span (menopause) and males do not is considered in evolutionary perspective. Two possible non-adaptive (incidental) explanations are discussed and rejected on available evidence. This sex difference is then considered as a possible adaptive response to differential parental investment tendencies of the two sexes. This hypothesis is evaluated in the context of sexual selection theory and the pattern of other observed sex differences in Homo sapiens. Finally, an attempt is made to explain the emergence of contemporary human investment patterns in terms of the changing patterns of parental certainty brought about by the Neolithic revolution. Cross-cultural data on investment patterns by subsistence type are used to test this hypothesis.     

Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan

Large, long-lived species experience more lifetime cell divisions and hence a greater risk of spontaneous tumor formation than smaller, short-lived species. Large, long-lived species are thus expected to evolve more elaborate tumor suppressor systems. In previous work, we showed that telomerase activity coevolves with body mass, but not lifespan, in rodents: telomerase activity is repressed in the somatic tissues of large rodent species but remains active in small ones. Without telomerase activity, the telomeres of replicating cells become progressively shorter until, at some critical length, cells stop dividing. Our findings therefore suggested that repression of telomerase activity mitigates the increased risk of cancer in larger-bodied species but not necessarily longer-lived ones. These findings imply that other tumor suppressor mechanisms must mitigate increased cancer risk in long-lived species. Here, we examined the proliferation of fibroblasts from 15 rodent species with diverse body sizes and lifespans. We show that, consistent with repressed telomerase activity, fibroblasts from large rodents undergo replicative senescence accompanied by telomere shortening and overexpression of p16(Ink4a) and p21(Cip1/Waf1) cycline-dependent kinase inhibitors. Interestingly, small rodents with different lifespans show a striking difference: cells from small shorter-lived species display continuous rapid proliferation, whereas cells from small long-lived species display continuous slow proliferation. We hypothesize that cells of small long-lived rodents, lacking replicative senescence, have evolved alternative tumor-suppressor mechanisms that prevent inappropriate cell division in vivo and slow cell growth in vitro. Thus, large-bodied species and small but long-lived species have evolved distinct tumor suppressor mechanisms.     

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.

     

Humpback whale (Megaptera novaeangliae) and killer whale (Orcinus orca) feeding aggregations for foraging on herring (Clupea harengus) in Northern Norway

Aggregations of predators on food patches have been documented for both terrestrial and marine animals. Here, we documented for the first time, and investigated, non-predatory aggregations occurring between humpback whales (Megaptera novaeangliae) and killer whales (Orcinus orca) while feeding on wintering Norwegian spring spawning herring (Clupea harengus) in Andfjord, northern Norway. Observational data were collected during 109 opportunistic surveys through three seasons 2013–2016. Killer whales were observed feeding on 59 occasions, with one to three humpback whales involved in 47 of these feeding events (79.7%), and there was an increased probability of finding feeding humpback whales when feeding killer whales also were observed. With killer whales identified as the initiating species in 94.4% of the feeding aggregations for which the first species was known, and with humpback whales joining and feeding on the fish ball afterwards, we suggest that humpback whales may benefit more from these aggregations than the opposite.     

Evolutionary senescence in plants

Senescence is a decline in age-specific survival and reproduction with advancing age. Studies of evolutionary plant senescence are designed to explain this decline in life history components within the context of natural selection. A review of studies of plant demography reveals senescent declines in both annual and perennial plants, but also suggests that there are some plant species which may not be expected to show senescence. Thus, future comparative studies of closely related species, with and without senescence, should be possible. The assumptions of the major evolutionary theories of senescence are evaluated for their validity with respect to plants. Different plant species violate one or more of the assumptions of the theories, yet the consequences of violating these assumptions have never been investigated. Whereas, to date, evolutionary senescence has been studied only indirectly in plants, it is concluded that plants provide good experimental systems for clarifying our understanding of senescence in natural populations.     

Mitochondrial sequence divergence among Antarctic killer whale ecotypes is consistent with multiple species

Recently, three visually distinct forms of killer whales (Orcinus orca) were described from Antarctic waters and designated as types A, B and C. Based on consistent differences in prey selection and habitat preferences, morphological divergence and apparent lack of interbreeding among these broadly sympatric forms, it was suggested that they may represent separate species. To evaluate this hypothesis, we compared complete sequences of the mitochondrial control region from 81 Antarctic killer whale samples, including 9 type A, 18 type B, 47 type C and 7 type-undetermined individuals. We found three fixed differences that separated type A from B and C, and a single fixed difference that separated type C from A and B. These results are consistent with reproductive isolation among the different forms, although caution is needed in drawing further conclusions. Despite dramatic differences in morphology and ecology, the relatively low levels of sequence divergence in Antarctic killer whales indicate that these evolutionary changes occurred relatively rapidly and recently.     

Termination of reproduction in nonhuman and human female primates

We examined demographic records from 13 captive primate species and a human population to determine age-related changes in female reproduction. In most species age-specific fertility declined and interbirth intervals increased with age. Using an operational definition of termination of reproduction based on individual variance in interbirth intervals, a proportion of females in most nonhuman species had terminated reproduction before death. Compared to other primates, a greater proportion of chimpanzees and human females ceased reproduction, and humans, in particular, were reproductively inactive for relatively longer than would be expected from their body weight. These empirical data quantify the extent of reproductive termination and thereby extend hitherto anecdotal accounts of this phenomenon in primates.