RESEARCH
Research
PUBLICATIONS
The following is a list of many of the CWR publications. New articles are added once available.
RECENT RESEARCH
Ellis, S., Franks, D.W., Nielsen, M.L.K., Weiss, M. N., and Croft, D. P. (2024).
The evolution of menopause in toothed whales. Nature, March 2024.
Abstract
Understanding how and why menopause has evolved is a long-standing challenge across disciplines. Females can typically maximize their reproductive success by reproducing for the whole of their adult life. In humans, however, women cease reproduction several decades before the end of their natural lifespan1,2. Although progress has been made in understanding the adaptive value of menopause in humans3,4, the generality of these findings remains unclear. Toothed whales are the only mammal taxon in which menopause has evolved several times5, providing a unique opportunity to test the theories of how and why menopause evolves in a comparative context. Here, we assemble and analyse a comparative database to test competing evolutionary hypotheses. We find that menopause evolved in toothed whales by females extending their lifespan without increasing their reproductive lifespan, as predicted by the ‘live-long’ hypotheses. We further show that menopause results in females increasing their opportunity for intergenerational help by increasing their lifespan overlap with their grandoffspring and offspring without increasing their reproductive overlap with their daughters. Our results provide an informative comparison for the evolution of human life history and demonstrate that the same pathway that led to menopause in humans can also explain the evolution of menopause in toothed whales.
Grimes, C., Brent, L. J. N., Ellis, S., Weiss, M. N., Franks, D. W., Ellifrit, D. K., and Croft, D. P. (2023).
Postreproductive female killer whales reduce socially inflicted injuries in their male offspring. Current Biology 33, 1–7.
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Summary
Understanding the evolution of menopause presents a long-standing scientific challenge—why should females cease ovulation prior to the end of their natural lifespan? In human societies, intergenerational resource transfers, for example, food sharing and caregiving, are thought to have played a key role in the evolution of menopause, providing a pathway by which postreproductive females can boost the fitness of their kin.To date however, other late-life contributions that postreproductive females may provide their kin have not been well studied. Here, we test the hypothesis that postreproductive female resident killer whales (Orcinus orca) provide social support to their offspring by reducing the socially inflicted injuries they experience. We found that socially inflicted injuries, as quantified by tooth rake marks, are lower for male offspring in the presence of their postreproductive mother. In contrast, we find no evidence that postreproductive mothers reduce rake marking in their daughters. Similarly, we find no evidence that either reproductive mothers or grandmothers (reproductive or postreproductive) reduce socially inflicted injuries in their offspring and grandoffspring, respectively. Moreover, we find that postreproductive females have no effect on reducing the rake marks for whales in their social unit who are not their offspring. Taken together, our results highlight that directing late-life support may be a key pathway by which postreproductive females transfer social benefits to their male offspring.
Nielsen, M. L. K., Ellis, S., Weiss, M. N., Towers, J. R., Doniol-Valcroze, T., Franks, D. W., Cant, M. A., Ellis, G. M., Ford, J. K. B., Malleson, M., Sutton, G., Shaw, T. J. H., Balcomb, K. C., Ellifrit, D. K., and Croft, D. P. (2023).
Temporal dynamics of mother–offspring relationships in Bigg’s killer whales: opportunities for kin-directed help by post-reproductive females. Proceedings of the Royal Society B, Volume 290 Issue 2000.
Abstract
Parents Age-related changes in the patterns of local relatedness (kinship dynamics)can be a significant selective force shaping the evolution of life historyand social behaviour. In humans and some species of toothed whales, averagefemale relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductiveconflict and benefits of late-life helping of kin. Killer whales (Orcinus orca)provide a valuable system for exploring social dynamics related to suchcosts and benefits in a mammal with an extended post-reproductive femalelifespan. We use more than 40 years of demographic and association data onthe mammal-eating Bigg’s killer whale to quantify how mother–offspringsocial relationships change with offspring age and identify opportunities forlate-life helping and the potential for an intergenerational reproductiveconflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg’s killer whales, with some variability inthe dispersal rate for both sexes. These patterns of dispersal provide opportu-nities for late-life helping particularly between mothers and their adult sons,while partly mitigating the costs of mother–daughter reproductive conflict.Our results provide an important step towards understanding why and howmenopause has evolved in Bigg’s killer whales.
Killer Whales
Ellis, S., Franks, D.W., Nielsen, M.L.K., Weiss, M. N., and Croft, D. P. (2024). The evolution of menopause in toothed whales. Nature, March 2024. Full Text.
Grimes, C., Brent, L. J. N., Ellis, S., Weiss, M. N., Franks, D. W., Ellifrit, D. K., and Croft, D. P. (2023). Postreproductive female killer whales reduce socially inflicted injuries in their male offspring. Current Biology 33, 1–7. Full Text.
Nielsen, M. L. K., Ellis, S., Weiss, M. N., Towers, J. R., Doniol-Valcroze, T., Franks, D. W., Cant, M. A., Ellis, G. M., Ford, J. K. B., Malleson, M., Sutton, G., Shaw, T. J. H., Balcomb, K. C., Ellifrit, D. K., and Croft, D. P. (2023). Temporal dynamics of mother–offspring relationships in Bigg’s killer whales: opportunities for kin-directed help by post-reproductive females. Proceedings of the Royal Society B, Volume 290 Issue 2000. Full Text.
Weiss, M. N., Ellis, S., Franks, D. W., Nielsen, M. L. K., Cant, M. A., Johnstone, R. A., Ellifrit, D. K., Balcomb, K. C., and Croft, D. P. (2023). Costly lifetime maternal investment in killer whales. Current Biology 33, 1–5. Full Text.
Grimes, C., Brent, L. J. N., Weiss, M. N., Franks, D. W., Balcomb, K. C., Ellifrit, D. K., Ellis, S., and Croft, D. P. (2022). The effect of age, sex, and resource abundance on patterns of rake markings in resident killer whales (Orcinus orca). Marine Mammal Science, 2022;1–18. Full Text.
Nielsen, M. L. K., Ellis, S., Towers, J. R., Doniol-Valcroze, T., Franks, D. W., Cant, M. A., Weiss, M. N., Johnstone, R. A., Balcomb, K. C., Ellifrit, D. K., and Croft, D. P. (2021). A long postreproductive life span is a shared trait among genetically distinct killer whale populations. Ecology and Evolution 11(13): 9123-9136. Full Text.
Weiss, M. N., Franks, D. W., Giles, D. A., Youngstrom, S., Wasser, S. K., Balcomb, K. C., Ellifrit, D. K., Domenici, P., Cant, M. A., Ellis, S., Nielsen, M. L. K., Grimes, C., and Croft, D. P. (2021). Age and sex influence social interactions, but not associations, within a killer whale pod. Proceedings of the Royal Society B, Volume 288 Issue 1953. Full Text.
Ellis, S., Franks, D. W., Weiss, M. N., Cant, M. A., Domenici, P., Balcomb, K. C., Ellifrit, D. K. and Croft, D. P. (2021) Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales. Behavioral Ecology and Sociobiology 75,
Article number: 75. Full Text.
Weiss, M. N., Franks, D. W., Balcomb, K. C., Ellifrit, D. K., Silk, M. J., Cant, M. A., and Croft, D. P. (2020). Modelling cetacean morbillivirus outbreaks in an endangered killer whale population. Biological Conservation 242: 108398. Full Text.
Nattrass, S., Croft, D. P., Ellis, S., Cant, M. A., Weiss, M. N., Wright, B, M., Stredulinsky, E., Doniol-Valcrozef, T., Ford, J. K. B., Balcomb, K. C., & Franks, D. W. (2019). Postreproductive killer whale grandmothers improve the survival of their grandoffspring. PNAS. Full Text.
Ellis, S., Franks, D. W., Nattrass, S., Currie, T. E., Cant, M. A., Giles, D., Balcomb, K. C., & Croft, D. P. (2018). Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales. Scientific Reports, 8(1). Full Text.
Ford, M. J., Parsons, K. M., Ward, E. J., Hempelmann, J. A., Emmons, C. K., Hanson, M. B., Balcomb, K. C., & Park, L. K. (2018). Inbreeding in an endangered killer whale population. Animal Conservation 21(5): 423-432. Full Text.
Ellis, S., Franks, D. W., Nattrass, S., Cant, M. A., Bradley, D. L., Giles, D., Balcomb, K. C., & Croft D. P. (2018). Postreproductive lifespans are rare in mammals. Ecology and Evolution 8(5): 2482-2494. Full Text.
Fearnbach, H., Durban, J. W., Ellifrit, D. K., & Balcomb, K. C. (2018). "Using aerial photogrammetry to detect changes in body condition of endangered southern resident killer whales." Endangered Species Research 35: 175-180. Full Text.
Ellis, S., Franks, D.W., Nattrass, S., Cant, M.A., Weiss, M.N., Giles, D., Balcomb, K.C., & Croft, D.P. (2017). Mortality risk and social network position in resident killer whales: sex differences and the importance of resource abundance. Proceedings of the Royal Society B: Biological Sciences, 284(1865), 20171313-20171313. Full Text.
Wasser, S. K., Lundin, J. I., Ayres, K., Seely, E., Giles, D., Balcomb, K., Hempelmann, J., Parsons, K., & Booth, R. (2017). Population growth is limited by nutritional impacts on pregnancy success in endangered Southern Resident killer whales (Orcinus orca). PloS One, 12(6), p.e0179824. Full Text.
Croft, D. P., Johnstone, R. A., Ellis, S., Nattrass, S., Franks, D. W., Brent, L. J. N., Mazzi, S., Balcomb, K. C., Ford, J. K. B., & Cant, M. A. (2017). Reproductive conflict and the evolution of menopause in killer whales. Current Biology, 27(2), 298–304. Full Text.
Lacy, R. C., Balcomb, K. C., Brent, L. J. N., Croft, D. P., Clark, C. W., & Paquet, P. C. (2016). Report on Population Viability Analysis model investigations of threats to the Southern Resident Killer Whale population from Trans-Mountain Expansion Project. Full Text.
Ward, E. J., Dahlheim, M. E., Waite, J. M., Emmons, C. K., Marshall, K. N., Chasco, B. E., & Balcomb, K. C. (2016). Long-distance migration of prey synchronizes demographic rates of top predators across broad spatial scales. Ecosphere, 7(2), e01276. Full Text.
Brent, L. J. N., Franks, D. W., Foster, E. A., Balcomb, K. C., Cant, M. A., & Croft, D. P. (2015). Ecological knowledge, leadership, and the evolution of menopause in killer whales. Current Biology, 25(6), 746–750. Full Text.
Cogan, J. (2015). 2015 Whale Sightings in the Salish Sea Central Salish Sea and Puget Sound. Center for Whale Research. Full Document.
Croft, D. P., Brent, L. J. N., Franks, D. W., & Cant, M. A. (2015). The evolution of prolonged life after reproduction. Trends in Ecology and Evolution, 30(7), 407–416. Full Text.
Foster, E. A., Franks, D. W., Mazzi, S., Darden, S. K., Balcomb, K. C., Ford, J. K. B., & Croft, D. P. (2012). Adaptive prolonged postreproductive life span in killer whales. Science, 337(6100), 1313–1313. Full Text.
Foster, E. A., Franks, D. W., Morrell, L. J., Balcomb, K. C., Parsons, K. M., van Ginneken, A., & Croft, D. P. (2012). Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Animal Behaviour, 83, 731–736. Full Text.
Fearnbach, H., Durban, J. W., Ellifrit, D. K., & Balcomb, K. C. (2011). Size and long-term growth trends of endangered fish-eating killer whales. Endangered Species Research, 13, 173–180. Full Text.
Ford, M. J., Hanson, M. B., Hempelmann, J. A., Ayres, K. L., Emmons, C. K., Schorr, G. S., Baird, R. W., Balcomb, K. C., Wasser, S. K., Parsons, K. M., Balcomb-Bartok, K. (2011). Inferred paternity and male reproductive success in a killer whale (Orcinus orca) population. Journal of Heredity, 102(5), 537–553. Full Text.
Ford, J. K. B., Ellis, G. M., Olesiuk, P. F., & Balcomb, K. C. (2010). Linking killer whale survival and prey abundance: food limitation in the oceans’ apex predator? Biology Letters, 6(1), 139–142. Full Text.
Parsons, K. M., Balcomb, K. C., Ford, J. K. B., & Durban, J. W. (2009). The social dynamics of southern resident killer whales and conservation implications for this endangered population. Animal Behaviour, 77(4), 963–971. Full Text.
Ward, E. J., Holmes, E. E., & Balcomb, K. C. (2009). Quantifying the effects of prey abundance on killer whale reproduction. Journal of Applied Ecology, 46(632–640). Full Text.
Ward, E. J., Parsons, K., Holmes, E. E., Balcomb Iii, K. C., & Ford, J. K. (2009). The role of menopause and reproductive senescence in a long-lived social mammal. Frontiers in Zoology, 6(4). Full Text.
Dahlheim, M. E., Schulman-Janiger, A., Black, N., Ternullo, R., Ellifrit, D., & Balcomb, K. C. (2008). Eastern temperate North Pacific offshore killer whales (Orcinus orca): Occurrence, movements, and insights into feeding ecology. Marine Mammal Science, 24(3), 719–729. Full Text.
Durban, J. W., & Parsons, K. M. (2006). Laser-metrics of free-ranging killer whales. Marine Mammal Science, 22(3), 732–743. Full Text.
Ford, J. K. B., & Ellis, G. M. (2005). Prey selection and food sharing by fish-eating “resident” killer whales (Orcinus orca) in British Columbia. Report to Fisheries and Oceans Canada. Full Text.
Ford, J. K. B., Ellis, G. M., Matkin, D. R., Balcomb, K. C., Briggs, D., & Morton, A. B. (2005). Killer whale attacks on minke whales: Prey capture and antipredator tactics. Marine Mammal Science, 21(4), 603–618. Full Text.
Ford, J. K. B., Ellis, G. M., & Olesiuk, P. F. (2005). Linking prey and population dynamics: did food limitation cause recent declines of “resident” killer whales (Orcinus orca) in British Columbia? Report to Fisheries and Oceans Canada. Full Text.
Gaydos, J. K., Balcomb, K. C., Osborne, R. W., & Dierauf, L. (2004). Evaluating potential infectious disease threats for southern resident killer whales, Orcinus orca: A model for endangered species. Biological Conservation, 117, 253–262. Full Text.
Krahn, M. M., Wade, P. R., Kalinowski, S. T., Dahlheim, M. E., Taylor, B. L., Hanson, M. B., Ylitalo, G. M., Angliss, R. P., Stein, J. E., & Waples, R. S. (2002). Status Review of Southern Resident Killer Whales (Orcinus orca) under the Endangered Species Act. NOAA Technical Memorandum NMFS Series. Full Text.
Ford, J. K. B., Ellis, G. M., & Balcomb, K. C. (2000). Killer Whales: The natural history and genealogy of Orcinus orca in British Columbia and Washington State, Second Edition. Vancouver, BC: UBC Press.
Ford, J. K. B., Ellis, G. M., Barrett-Lennard, L. G., Morton, A. B., Palm, R. S., & Balcomb, K. C. (1998). Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Canadian Journal of Zoology, 76, 1456–1471. Full Text.
Dahlheim, M. E., Ellifrit, D. K., & J. D. Swenson. (1997). Killer whales of southeast Alaska: A catalogue of photo-identified individuals. Full Text.
Brault, S., & Caswell, H. (1993). Pod-specific demography of killer whales (Orcinus orca). Ecology, 74(745), 1444–1454. Full Text.
Bigg, M. A. (1990). Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. In P. Hammond, S. Mizroch, & G. Donovan (Eds.), Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters (pp. 383–405). Cambridge. Full Text.
Olesiuk, P. F., Bigg, M. A., & Ellis, G. M. (1990). Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. In P. S. Hammond, S. A. Mizroch, & G. P. Donovan (Eds.), Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters (pp. 209–243). Cambridge. Full Text.
Bigg, M. A. (1987). Killer Whales: A Study of Their Identification, Genealogy and Natural History in British Columbia and Washington State. Nanaimo: Phantom Press.
Balcomb, K. C., & Bigg, M. A. (1986). Population biology of three resident killer whale pods in Puget Sound and off southern Vancouver Island. In B. C. Kirkevold & J. S. Lockard (Eds.), Behavioral Biology of Killer Whales (pp. 85–95). Alan R. Liss, Inc.
Heimlich-Boran, J. R. (1986). Behavioral ecology of killer whales (Orcinus orca) in the Pacific Northwest. Canadian Journal of Zoology, 66, 565–578. Full Text.
Dolphins
Fearnbach, H., Durban, J., Parsons, K., & Claridge, A. D. (2012). Photographic mark–recapture analysis of local dynamics within an open population of dolphins. Ecological Applications, 22(5), 1689–1700. Full Text.
Fearnbach, H., Durban, J., Parsons, K., & Claridge, D. (2012). Seasonality of calving and predation risk in bottlenose dolphins on Little Bahama Bank. Marine Mammal Science, 28(2), 402–411.
Parsons, K. M., Durban, J. W., Claridge, D. E., Herzing, D. L., Balcomb, K. C., & Noble, L. R. (2006). Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the northern Bahamas. Marine Mammal Science, 22(2), 276–298. Full Text.
Parsons, K. M., Durban, J. W., Claridge, D. E., Balcomb, K. C., Noble, L. R., & Thompson, P. M. (2003). Kinship as a basis for alliance formation between male bottlenose dolphins, Tursiops truncatus, in the Bahamas. Animal Behavior, 66, 185–194.
Parsons, K. M. (2001). Reliable microsatellite genotyping of dolphin DNA from faeces. Molecular Ecology Notes, 1, 341–344.
Durban, J. W., Parsons, K. M., Claridge, D. E., & Balcomb, K. C. (2000). Quantifying Dolphin Occupancy Patterns. Marine Mammal Science, 16(4), 825–828.
Parsons, K. M., Dallas, J. F., Claridge, D. E., Durban, J. W., Balcomb, K. C., Thompson, P. M., & Noble, L. R. (1999). Amplifying dolphin mitochondrial DNA from faecal plumes. Molecular Ecology, 8, 1753–1768.
Claridge, D. E. (1994). Photo-identification study to assess the population size of Atlantic bottlenose dolphins in central Abaco. Bahamas. Journal of Science, 1, 12–16.
Humpback Whales
Calambokidis, J., Steiger, G., Straley, J., Herman, L., Cerchio, S., Salden, D., Urban R., J., Jacobsen, J., von Ziegesar, O., Balcomb, K. C., Gabriele, C., Dahlheim, M., Uchida, S., Ellis, G., Miyamura, Y., de Guevara P., P. L., Yamaguchi, M., Sato, F., Mizroch, S., Schlender, L., Barlow, J., & Quinn II, T. (2001). Movements and population structure of humpback whales in the North Pacific. Marine Mammal Science, 17(4), 769–794.
Calambokidis, J., Steigerl, G. H., Rasmussenl, K., Urban, J. R., Ladron de Guevara, P. P., Salinas, M., Jacobsen, J. K., Scott Baker, C., & Herman, L. M. (2000). Migratory destinations of humpback whales that feed off California, Oregon and Washington. Marine Ecology Progress Series, 192, 295–304.
Urban, J., Alvarez, C., Salinas, M., Jacobsen, J., Balcomb, K. C., Jaramillo, A., de Guevara, P. L., & Aguayo, A. (1999). Population size of humpback whale, Megaptera novaeangliae, in waters off the Pacific coast of Mexico. Fishery Bulletin, 97, 1017–1024.
Calambokidis, J., Steiger, G. H., Evenson, J. R., Flynn, K. R., Balcomb, K. C., Claridge, D. E., Bloedel, P., Straley, J.M., Baker, C.S., von Ziegesar, O., Dahlheim, M. E., Waite, J. M., Darling, J. D., Ellis, G., & Green, G. (1996). Interchange and isolation of humpback whales off California and other North Pacific feeding grounds. Marine Mammal Science, 12(2), 215–226.
Darling, J. D., Calambokidis, J., Balcomb, K. C., Bloedel, P., Flynn, K., Mochizuki, A., Mori, K., Sato, F., Suganuma, H., & Yamaguchi, M. (1996). Movement of a humpback whale (Megaptera novaeangliae) from Japan to British Columbia and return. Marine Mammal Science, 12(2), 281–287.
Steiger, G., Calambokidis, J., Sears, R., Balcomb, K. C., & Cubbage, J. (1991). Movement of humpback whales between California and Costa Rica. Marine Mammal Science,7(3), 306–310.
Calambokidis, J., Cubbage, J. C., Steiger, G. H., Balcomb, K. C., & Bloedel, P. (1990). Population estimates of humpback whales in the Gulf of the Farralones, California. In P. S. Hammond, S. A. Mizroch, & G. P. Donovan (Eds.), Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters (pp. 325–328). Cambridge.
Blue Whales
Calambokidis, J., Steiger, G. H., Cubbage, J. C., Balcomb, K. C., Ewald, C., Kruse, S., Wells, R., & Sears, R. (1990). Sightings and movements of blue whales off central California 1986-1988 from photo-identification of individuals. In P. S. Hammond, S. A. Mizroch, & G. P. Donovan (Eds.), Individual Recognition of Cetaceans: Use of Photo-Identification and Other Techniques to Estimate Population Parameters (pp. 343–349). Cambridge
Beaked Whales
Cox, T. M., Ragen, T. J., Read, A. J., Vos, E., Baird, R. W., Balcomb, K. C., Barlow, J., Caldwell, J., Cranford, T., Crum, L., D’amico, A., D’Spain, G., Fernandez, A., Finneran, J., Gentry, R., Gerth, W., Gullands, F., Hilderbrand, J., Houserp, D., Hullar, T., Jepson, P. D., Ketten, D., Macleod, C. D., Miller, P., Moore, S., Mountain, D. C., Palka, D., Ponganis, P., Rommel, S., Rowles, T., Taylor, B., Tyack, P., Wartzok, D., Gisiner, R., Meads, J., & Benner, L. (2006). Understanding the impacts of anthropogenic sound on beaked whales. Journal of Cetacean Resource Management, 7(3), 177–187.
General Cetaceans
Durban, J. W., Elston, D. A., Ellifrit, D. K., Dickson, E., Hammond, P. S., & Thompson, P. M. (2005). Multi-site mark-recapture for cetaceans: population estimates with Bayesian model averaging. Marine Mammal Science, 2(1), 80–92.
Durban, J. W., & Elston, D. A. (2005). Mark–recapture with occasion and individual effects: abundance estimation through bayesian model selection in a fixed dimensional parameter space. Journal of Agricultural, Biological and Environmental Statistics,10(3), 291–305. Full Text.
Parsons, K. M., & Durban, J. W. (2003). Comparing two alternative methods for sampling small cetaceans for molecular analysis. Marine Mammal Science, 19(1), 224–231.