Postreproductive killer whale grandmothers improve the survival of their grandoffspring.
ABSTRACT: Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales.
Project description:Usually animals reproduce into old age, but a few species such as humans and killer whales can live decades after their last reproduction. The grandmother hypothesis proposes that such life-history evolved through older females switching to invest in their existing (grand)offspring, thereby increasing their inclusive fitness and selection for post-reproductive lifespan. However, positive grandmother effects are also found in non-menopausal taxa, but evidence of their associated fitness effects is rare and only a few tests of the hypothesis in such species exist. Here we investigate the grandmother effects in Asian elephants. Using a multigenerational demographic dataset on semi-captive elephants in Myanmar, we found that grandcalves from young mothers (<20 years) had 8 times lower mortality risk if the grandmother resided with her grandcalf compared to grandmothers residing elsewhere. Resident grandmothers also decreased their daughters' inter-birth intervals by one year. In contrast to the hypothesis predictions, the grandmother's own reproductive status did not modify such grandmother benefits. That elephant grandmothers increased their inclusive fitness by enhancing their daughter's reproductive rate and success irrespective of their own reproductive status suggests that fitness-enhancing grandmaternal effects are widespread, and challenge the view that grandmother effects alone select for menopause coupled with long post-reproductive lifespan.
Project description:A substantial period of life after reproduction ends, known as postreproductive lifespan (PRLS), is at odds with classical life history theory and its causes and mechanisms have puzzled evolutionary biologists for decades. Prolonged PRLS has been confirmed in only two non-human mammals, both odontocete cetaceans in the family Delphinidae. We investigate the evidence for PRLS in a third species, the false killer whale, Pseudorca crassidens, using a quantitative measure of PRLS and morphological evidence from reproductive tissues.We examined specimens from false killer whales from combined strandings (South Africa, 1981) and harvest (Japan 1979-80) and found morphological evidence of changes in the activity of the ovaries in relation to age. Ovulation had ceased in 50% of whales over 45 years, and all whales over 55 years old had ovaries classified as postreproductive. We also calculated a measure of PRLS, known as postreproductive representation (PrR) as an indication of the effect of inter-population demographic variability. PrR for the combined sample was 0.14, whereas the mean of the simulated distribution for PrR under the null hypothesis of no PRLS was 0.02. The 99th percentile of the simulated distribution was 0.08 and no simulated value exceeded 0.13. These results suggest that PrR was convincingly different from the measures simulated under the null hypothesis.We found morphological and statistical evidence for PRLS in South African and Japanese pods of false killer whales, suggesting that this species is the third non-human mammal in which this phenomenon has been demonstrated in wild populations. Nonetheless, our estimate for PrR in false killer whales (0.14) is lower than the single values available for the short-finned pilot whale (0.28) and the killer whale (0.22) and is more similar to working Asian elephants (0.13).
Project description:In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species - humans, killer whales and short-finned pilot whales - have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. Of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild.
Project description:BACKGROUND:The existence of extended post-reproductive lifespan is an evolutionary puzzle, and its taxonomic prevalence is debated. One way of measuring post-reproductive life is with post-reproductive representation, the proportion of adult years lived by females after cessation of reproduction. Analyses of post-reproductive representation in mammals have claimed that only humans and some toothed whale species exhibit extended post-reproductive life, but there are suggestions of a post-reproductive stage for false killer whales and Asian elephants. Here, we investigate the presence of post-reproductive lifespan in Asian elephants using an extended demographic dataset collected from semi-captive timber elephants in Myanmar. Furthermore, we investigate the sensitivity of post-reproductive representation values to availability of long-term data over 50 years. RESULTS:We find support for the presence of an extended post-reproductive stage in Asian elephants, and that post-reproductive representation and its underlying demographic rates depend on the length of study period in a long-lived animal. CONCLUSIONS:The extended post-reproductive lifespan is unlikely due to physiological reproductive cessation, and may instead be driven by mating preferences or condition-dependent fertility. Our results also show that it is crucial to revisit such population measures in long-lived species as more data is collected, and if the typical lifespan of the species exceeds the initial study period.
Project description:Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the "paternal grandmother age effect" (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model.IMPORTANCE Unidirectional cytoplasmic incompatibility (CI) results in a postfertilization incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.
Project description:Franks et al. (2016) consider that the degree of error in estimated ages used to define survivorship patterns of northern and southern resident killer whale ( Orcinus orca ) populations is of insignificant impact to estimates of the species' postreproductive lifespan (PRLS). We provide evidence that survival probabilities for killer whales using a dataset comprising estimated age animals differ significantly from that determined using data collected from known-age animals in the Pacific Northwest over the past 40 years. Consequently, our findings indicate that the degree of error in age estimates and ensuing survivorship patterns do not support the notion by Franks et al. (2016) of a prolonged PRLS in the female killer whale that is comparable to the PRLS observed in humans.
Project description:The MOXD2 gene encodes a membrane-bound monooxygenase similar to dopamine-?-hydroxylase, and has been proposed to be associated with olfaction. In this study, we analyzed MOXD2 genes from 64 mammalian species, and identified loss-of-function mutations in apes (humans, Sumatran and Bornean orangutans, and five gibbon species from the four major gibbon genera), toothed whales (killer whales, bottlenose dolphins, finless porpoises, baijis, and sperm whales), and baleen whales (minke whales and fin whales). We also identified a shared 13-nt deletion in the last exon of Old World cercopithecine monkeys that results in conversion of a membrane-bound protein to a soluble form. We hypothesize that the frequent inactivation and alteration of MOXD2 genes in catarrhines and whales may be associated with the evolution of olfaction in these clades.
Project description:INTRODUCTION:Early childhood interventions primarily focus on the mother-child relationship, but grandmothers are often critical in childcare in low-resource settings. Prior research is mixed on how grandmother involvement influences child outcomes and there is a paucity of research on grandmother caregiving in low-income and middle-income countries. We examined the role of grandmother involvement on child growth and development in the first 2 years of life cross sectionally and longitudinally in rural Pakistan. METHODS:We used data from the Bachpan Cohort, a longitudinal birth cohort in rural Pakistan. Maternally reported grandmother involvement in daily instrumental and non-instrumental caregiving was collected at 3 and 12 months. A summed score was created and categorised into non-involved, low and high. Outcomes included 12-month and 24-month child growth, 12-month Bayley Scales of Infant and Toddler Development and 24-month Ages and Stages Questionnaire-Socioemotional. We used multivariable generalised linear models to estimate mean differences (MD) at 12 months (n=727) and 24 months (n=712). Inverse probability weighting was used to account for missingness and sampling. RESULTS:In our sample, 68% of children lived with a grandmother, and most grandmothers were involved in caregiving. Greater 3-month grandmother involvement was positively associated with 12-month weight z-scores; however, greater involvement was associated with lower 24-month weight z-scores. High 12-month grandmother involvement was associated with improved 12-month cognitive (MD=0.38, 95% CI -0.01 to 0.76), fine motor skills (MD=0.45, 95% CI 0.08 to 0.83) and 24-month socioemotional development (MD=-17.83, 95% CI -31.47 to -4.19). No meaningful associations were found for length z-scores or language development. CONCLUSION:In rural Pakistan, grandmothers provide caregiving that influences early child development. Our findings highlight the complex relationship between grandmother involvement and child weight, and suggest that grandmothers may positively promote early child cognitive, fine motor and socioemotional development. Understanding how grandmother involvement affects child outcomes in early life is necessary to inform caregiving interventions.
Project description:Grandmothers provide key care to their grandchildren in both contemporary and historic human populations. The length of the grandmother-grandchild relationship provides a basis for such interactions, but its variation and determinants have rarely been studied in different contexts, despite changes in age-specific mortality and fertility rates likely having affected grandmotherhood patterns across the demographic transition. Understanding how often and long grandmothers have been available for their grandchildren in different conditions may help explain the large differences between grandmaternal effects found in different societies, and is vital for developing theories concerning the evolution of menopause, post-reproductive longevity, and family living. Using an extensive genealogical dataset from Finland spanning the demographic transition, we quantify the length of grandmotherhood and its determinants from 1790-1959. We found that shared time between grandmothers and grandchildren was consistently low before the demographic transition, only increasing greatly during the 20th century. Whilst reduced childhood mortality and increasing adult longevity had a role in this change, grandmaternal age at birth remained consistent across the study period. Our findings further understanding of the temporal context of grandmother-grandchild relationships, and emphasise the need to consider the demography of grandmotherhood in a number of disciplines, including biology (e.g. evolution of the family), sociology (e.g. changing family structures), population health (e.g. changing age structures), and economics (e.g. workforce retention).
Project description:The costs of predation may exert significant pressure on the mode of communication used by an animal, and many species balance the benefits of communication (e.g. mate attraction) against the potential risk of predation. Four groups of toothed whales have independently evolved narrowband high-frequency (NBHF) echolocation signals. These signals help NBHF species avoid predation through acoustic crypsis by echolocating and communicating at frequencies inaudible to predators such as mammal-eating killer whales. Heaviside's dolphins (Cephalorhynchus heavisidii) are thought to exclusively produce NBHF echolocation clicks with a centroid frequency around 125 kHz and little to no energy below 100 kHz. To test this, we recorded wild Heaviside's dolphins in a sheltered bay in Namibia. We demonstrate that Heaviside's dolphins produce a second type of click with lower frequency and broader bandwidth in a frequency range that is audible to killer whales. These clicks are used in burst-pulses and occasional click series but not foraging buzzes. We evaluate three different hypotheses and conclude that the most likely benefit of these clicks is to decrease transmission directivity and increase conspecific communication range. The expected increase in active space depends on background noise but ranges from 2.5 (Wenz Sea State 6) to 5 times (Wenz Sea State 1) the active space of NBHF signals. This dual click strategy therefore allows these social dolphins to maintain acoustic crypsis during navigation and foraging, and to selectively relax their crypsis to facilitate communication with conspecifics.