- Email: [email protected]
Social Evolution: Uneasy Lies the Head
Current Biology
Dispatches Social Evolution: Uneasy Lies the Head Andrew F.G. Bourke School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.09.071
Inclusive fitness theory explains why workers in insect societies sometimes kill their queen. As the theory predicts, workers in a wasp species are more likely to act matricidally when more highly related to potential worker offspring. Is a social insect colony like a piece of clockwork, a set of smoothly meshing parts all working together towards a shared goal? Or is it like a sackful of fighting ferrets, a haphazardly throwntogether collection of individuals each with only self-interest in mind? The reality, of course, sits across a broad range in between, which is why insect sociality is of special interest and serves as a model for the emergence of biological organisation at all evolutionary levels [1,2]. One of the great strengths of Hamilton’s [3] inclusive fitness theory (kin selection) is that it provides tools with which to understand exactly how, in insect societies and beyond, cooperation and conflict can coexist. In the theory, cooperation arises when group members share a common evolutionary interest, often through their occurring in families of some kind and thereby sharing genes. Conflict arises because group members may be unequally related to offspring, with the result that their evolutionary interests fail to overlap completely [4,5]. Inclusive fitness theory therefore predicts that the balance of cooperation and conflict, being dependent on the extent of fitness overlap, should vary with context. A case in point is worker matricide in the eusocial Hymenoptera (ants, bees and wasps with a sterile or partially-sterile worker caste). Worker matricide occurs when, as observed in some bees and wasps, workers kill their mother queen [4,6]. A new study by Kevin Loope shows for the first time that whether workers of the wasp Dolichovespula arenaria take this extreme measure depends on context, and specifically the colony’s kin structure, in a manner predicted by inclusive fitness theory [7]. In eusocial Hymenoptera, workers are not always completely sterile, and in
some species can lay unfertilised eggs. Because Hymenoptera are haplodiploid (such that females are diploid and develop from fertilised eggs and males are haploid and develop from unfertilised eggs), workers’ eggs give rise to viable adult males. In a colony headed by one, singly-mated queen, the queen is more closely related to her sons (relatedness, r = 0.5) than to the workers’ sons, her grandsons (r = 0.25). However, workers are more closely related to their own (r = 0.5) or other workers’ sons (r = 0.375) than to the queen’s sons, their brothers (r = 0.25). Inclusive fitness theory therefore predicts potential queen– worker conflict over male production, with each party favouring the production of its own males [4]. Consistent with this, worker reproduction is widely associated with mutual egg-eating and aggression between queens and workers [5,8]. Trivers and Hare [4] first discussed how such conflict might escalate into worker matricide, so permitting workers to reproduce free from queen interference. These authors also suggested that worker matricide should occur in a contextdependent manner. For example, within annual colonies, matricide should be more likely after the colony has switched from worker production to sexual (queen and male) production, because workers killing a worker-producing queen would lose a greater number of future sibs [4]. These insights were extended by later authors [8–10] and a full model of worker matricide was presented by Bourke [6]. Among other cases, this model considered the effect of multiple mating (polyandry) by the queen on the likelihood of matricide. Polyandry reduces the relatedness of the average (non-laying) worker to other workers and hence to other workers’ sons [10]. So the model concluded that polyandry would reduce
the inclusive fitness gain to workers from matricide and hence make matricide less likely [6]. Foster and Ratnieks [11] provided comparative support for this prediction by showing that, in vespine wasps, species with the least polyandry (highest worker–worker relatedness) had the highest frequencies of queenless nests. However, although evidence of worker matricide in annual bees and wasps has continued to accumulate [12–14], detailed empirical studies of its causes have been lacking. This is essentially because of the practical challenges of trying to observe what, for all parties, is a rare (indeed once-in-alifetime) event. Loope [7] presents the first detailed empirical study of worker matricide and shows that the predicted association with high worker–worker relatedness is found in D. arenaria. D. arenaria is a common yellowjacket wasp of North America, forming annual colonies of up to several hundred workers. Queens (Figure 1) are facultatively polyandrous, with some queens mating with two or more males, and workers are capable of worker maleproduction [15]. In Loope’s [7] study population in New York State, USA, 42% of colonies were queenless (excluding incipient and senescing colonies). By bringing colonies into the laboratory and painstakingly filming them in observation boxes, Loope [7] observed worker matricide of the queen in three cases. In each, a single worker began to sting the queen, and in two cases this worker was joined by others in its attack. Although the queen sometimes defended herself, in all three cases only the queen died. Hence the queen should indeed lie uneasy, because her own daughters may prove to be her assassins. These observations, together with estimates suggesting that intrinsic queen mortality is
Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved R1077
Current Biology
Dispatches
Figure 1. Queen Dolichovespula arenaria wasp in the nest.
D. arenaria queens, including this marked one, risk being killed by their own worker daughters. (Photo credit: Kevin Loope.)
low, led to the inference that almost all (c. 90%) of queenlessness in mature, presenescence colonies was caused by worker matricide. Loope [7] next carried out a detailed genetic analysis using polymorphic microsatellite markers of a sample of 21 colonies collected from the field. This yielded measures of the level of worker– worker relatedness, which turned out to vary with both mating frequency and the extent to which, in offspring of polyandrous queens, the queen’s mates shared paternity (paternity skew). An analysis then revealed that worker–worker relatedness was associated with a colony’s queen status, being significantly higher in queenless than in queenright colonies (r = 0.69 v. 0.52, respectively). In short, queenlessness, the primary cause of which is worker matricide, occurred preferentially in colonies where workers would be most closely related to workerproduced males. This matched the prediction from inclusive fitness theory [6]. The conclusion that the kin structure of the colony causally affects the likelihood of worker matricide rests on ruling out plausible alternative explanations for the association of high relatedness with queenlessness. In this respect, Loope’s [7] study makes a strong case. For example, one possibility is that highrelatedness colonies contained inbred
queens likely to produce diploid males and thereby induced worker matricide. In Hymenoptera, haplodiploidy is associated with a system of sex determination in which homozygosity at a sex-determining locus, which may stem from inbreeding, creates diploid males. As these male are sterile, they represent a substantial cost to the colony [16] and workers might benefit from eliminating queens producing such males. However, in the present study, singly-mated D. arenaria queens had not inbred, ruling out this explanation [7]. Furthermore, a colony’s stage in the colony cycle, implicated in explaining differences in levels of worker male production in queenright conditions in another Dolichovespula species [17], did not explain the association found. Most tellingly, high worker–worker relatedness did not always arise from single queen mating in D. arenaria. In some colonies, it arose because polyandrous queens exhibited high paternity skew, so elevating relatedness among their worker offspring. Such skewed paternity could itself be a response to an inbred pairing between the queen and at least one of her mates [7]. Regardless, an analysis showed that, among polyandrous queens, paternity skew was significantly higher in queenless than in queenright colonies [7]. This result was as expected
if high relatedness stemming from high paternity skew induced matricide and suggested that relatedness, not mating frequency per se, underlies the association with matricide. It is also consistent with workers assessing their colony’s kin structure from chemical cues covarying with nestmate relatedness, as suggested in other eusocial insects [18], rather than directly from the queen’s mating frequency [7]. Loope’s [7] fine study breaks new ground by taking research on worker matricide firmly into the empirical realm. Although experimental confirmation of its inferences lie in the future, it provides very strong evidence for inclusive fitness theory’s predicted link between worker–worker relatedness and matricide. In so doing, it further rebuts recent criticism of the utility of the theory [19,20] and shows how cooperation, depending on context, can degenerate into conflict in ways the theory predicts. REFERENCES 1. Bourke, A.F.G. (2011). Principles of Social Evolution (Oxford: Oxford University Press). 2. West, S.A., Fisher, R.M., Gardner, A., and Kiers, E.T. (2015). Major evolutionary transitions in individuality. Proc. Natl. Acad. Sci. USA 112, 10112–10119. 3. Hamilton, W.D. (1964). The genetical evolution of social behaviour I, II. J. Theor. Biol. 7, 1–52. 4. Trivers, R.L., and Hare, H. (1976). Haplodiploidy and the evolution of the social insects. Science 191, 249–263. 5. Ratnieks, F.L.W., Foster, K.R., and Wenseleers, T. (2006). Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581–608. 6. Bourke, A.F.G. (1994). Worker matricide in social bees and wasps. J. Theor. Biol. 167, 283–292. 7. Loope, K.J. (2015). Queen killing is linked to high worker-worker relatedness in a social wasp. Curr. Biol. 25, 2976–2979. 8. Bourke, A.F.G. (1988). Worker reproduction in the higher eusocial Hymenoptera. Q. Rev. Biol. 63, 291–311. 9. Bulmer, M.G. (1983). The significance of protandry in social Hymenoptera. Am. Nat. 121, 540–551. 10. Ratnieks, F.L.W. (1988). Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217–236. 11. Foster, K.R., and Ratnieks, F.L.W. (2001). Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav. Ecol. Sociobiol. 50, 1–8.
R1078 Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved
Current Biology
Dispatches 12. Bloch, G., and Hefetz, A. (1999). Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies. Behav. Ecol. Sociobiol. 45, 125–135. 13. Strassmann, J.E., Nguyen, J.S., Are´valo, E., Cervo, R., Zacchi, F., Turillazzi, S., and Queller, D.C. (2003). Worker interests and male production in Polistes gallicus, a Mediterranean social wasp. J. Evol. Biol. 16, 254–259. 14. Soro, A., Ayasse, M., Zobel, M.U., and Paxton, R.J. (2009). Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insectes Soc. 56, 55–63.
15. Freiburger, B.J., Breed, M.D., and Metcalf, J.L. (2004). Mating frequency, within-colony relatedness and male production in a yellow jacket wasp, Dolichovespula arenaria. Mol. Ecol. 13, 3703–3707.
18. Boomsma, J.J., Nielsen, J., Sundstro¨m, L., Oldham, N.J., Tentschert, J., Petersen, H.C., and Morgan, E.D. (2003). Informational constraints on optimal sex allocation in ants. Proc. Natl. Acad. Sci. USA 100, 8799–8804.
16. Cook, J.M., and Crozier, R.H. (1995). Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10, 281–286.
19. Nowak, M.A., Tarnita, C.E., and Wilson, E.O. (2010). The evolution of eusociality. Nature 466, 1057–1062.
17. Bonckaert, W., Van Zweden, J.S., D’Ettorre, P., Billen, J., and Wenseleers, T. (2011). Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp. Mol. Ecol. 20, 3455–3468.
20. Abbot, P., Abe, J., Alcock, J., Alizon, S., Alpedrinha, J.A.C., Andersson, M., Andre, J.B., van Baalen, M., Balloux, F., Balshine, S., et al. (2011). Inclusive fitness theory and eusociality. Nature 471, E1–E4.
Animal Evolution: Only Rocks Can Set the Clock Davide Pisani1,2,* and Alexander G. Liu2 1School
of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK of Earth Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.10.015 2School
Molecular clocks have become the method of choice to date the tree of life. A new study demonstrates that there are limits to their precision, which may only be overcome by improving our knowledge of the fossil record. When did animals (the Metazoa) evolve [1–4]? Can we correlate the evolutionary history of animals with specific events in Earth history to understand what drove their origin and subsequent diversification [1–4]? For example, was the origin of animals triggered by the emergence of modern, well-oxygenated oceans [5], or did oxygenated oceans emerge as a consequence of the evolution of spongelike animals capable of removing dissolved carbon from the water column and sequestering it within sediments [6,7]? These and other similar questions have fascinated scientists for generations, and are united by the requirement of an accurate and precise timescale of animal evolution to answer them. Attempts to offer such a timescale often utilise methods based on the molecular clock. The molecular clock — first proposed by Emile Zuckerkandl and Linus Pauling in 1962 — works on the premise that the number of mutations independently accumulating in the genomes of living organisms is to some level proportional to the time that has elapsed since they shared a common ancestor [8]. However, a new study by dos Reis and colleagues [1]
in this issue of Current Biology demonstrates that, at present, these methods are not precise enough to correlate milestones in early animal history with events in the geological record. Scientists have long relied on fossils to draft a timescale of animal evolution, but the fossil record is beset by several rather annoying flaws. Due to the vagaries of sedimentary, tectonic and erosive processes, the fossil record is incomplete [9]. Furthermore, the oldest known fossil of a given species identifies only its first appearance in the rock record, which generally corresponds to a time when the species was already well established, with stable and abundant populations. The biological origin of a given species will always be older than its first appearance in the fossil record [10]. Finally, the deeper we delve into Earth history, the harder it becomes to recognise specific fossils as the extinct relatives of living species. DNA and proteins do not preserve well, and the genealogical relationships of fossils close to the root of the animal tree can only be defined by the presence of shared morphological features (homologies). Yet,
the further we move back in time, the smaller the number of homologies becomes [2]. As a result, whereas we can intuitively visualise the appearance of the last common ancestor of, say, humans and chimps, an animal that lived 6.5– 10 million years ago [10], picturing the last common ancestor of humans and sea cucumbers (an animal that inhabited the Earth’s oceans at least 515.5 million years ago [1–4,10]) is rather more speculative. Even experts, when faced with the fossil remains of the very first animals, struggle to confidently identify them as such, simply because they have no clear idea of what these animals were supposed to look like. Such uncertainties have shrouded the earliest history of animals in mystery. Currently, the best candidates for the oldest possible animal fossils are members of the diverse and largely softbodied Ediacaran macrobiota, found in rocks dated to 580–541 million years ago [11]. However, many of these organisms have proven difficult to interpret, with little agreement as to whether iconic taxa such as Dickinsonia, Fractofusus, or Spriggina (Figure 1) are
Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved R1079
Dispatches Social Evolution: Uneasy Lies the Head Andrew F.G. Bourke School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.09.071
Inclusive fitness theory explains why workers in insect societies sometimes kill their queen. As the theory predicts, workers in a wasp species are more likely to act matricidally when more highly related to potential worker offspring. Is a social insect colony like a piece of clockwork, a set of smoothly meshing parts all working together towards a shared goal? Or is it like a sackful of fighting ferrets, a haphazardly throwntogether collection of individuals each with only self-interest in mind? The reality, of course, sits across a broad range in between, which is why insect sociality is of special interest and serves as a model for the emergence of biological organisation at all evolutionary levels [1,2]. One of the great strengths of Hamilton’s [3] inclusive fitness theory (kin selection) is that it provides tools with which to understand exactly how, in insect societies and beyond, cooperation and conflict can coexist. In the theory, cooperation arises when group members share a common evolutionary interest, often through their occurring in families of some kind and thereby sharing genes. Conflict arises because group members may be unequally related to offspring, with the result that their evolutionary interests fail to overlap completely [4,5]. Inclusive fitness theory therefore predicts that the balance of cooperation and conflict, being dependent on the extent of fitness overlap, should vary with context. A case in point is worker matricide in the eusocial Hymenoptera (ants, bees and wasps with a sterile or partially-sterile worker caste). Worker matricide occurs when, as observed in some bees and wasps, workers kill their mother queen [4,6]. A new study by Kevin Loope shows for the first time that whether workers of the wasp Dolichovespula arenaria take this extreme measure depends on context, and specifically the colony’s kin structure, in a manner predicted by inclusive fitness theory [7]. In eusocial Hymenoptera, workers are not always completely sterile, and in
some species can lay unfertilised eggs. Because Hymenoptera are haplodiploid (such that females are diploid and develop from fertilised eggs and males are haploid and develop from unfertilised eggs), workers’ eggs give rise to viable adult males. In a colony headed by one, singly-mated queen, the queen is more closely related to her sons (relatedness, r = 0.5) than to the workers’ sons, her grandsons (r = 0.25). However, workers are more closely related to their own (r = 0.5) or other workers’ sons (r = 0.375) than to the queen’s sons, their brothers (r = 0.25). Inclusive fitness theory therefore predicts potential queen– worker conflict over male production, with each party favouring the production of its own males [4]. Consistent with this, worker reproduction is widely associated with mutual egg-eating and aggression between queens and workers [5,8]. Trivers and Hare [4] first discussed how such conflict might escalate into worker matricide, so permitting workers to reproduce free from queen interference. These authors also suggested that worker matricide should occur in a contextdependent manner. For example, within annual colonies, matricide should be more likely after the colony has switched from worker production to sexual (queen and male) production, because workers killing a worker-producing queen would lose a greater number of future sibs [4]. These insights were extended by later authors [8–10] and a full model of worker matricide was presented by Bourke [6]. Among other cases, this model considered the effect of multiple mating (polyandry) by the queen on the likelihood of matricide. Polyandry reduces the relatedness of the average (non-laying) worker to other workers and hence to other workers’ sons [10]. So the model concluded that polyandry would reduce
the inclusive fitness gain to workers from matricide and hence make matricide less likely [6]. Foster and Ratnieks [11] provided comparative support for this prediction by showing that, in vespine wasps, species with the least polyandry (highest worker–worker relatedness) had the highest frequencies of queenless nests. However, although evidence of worker matricide in annual bees and wasps has continued to accumulate [12–14], detailed empirical studies of its causes have been lacking. This is essentially because of the practical challenges of trying to observe what, for all parties, is a rare (indeed once-in-alifetime) event. Loope [7] presents the first detailed empirical study of worker matricide and shows that the predicted association with high worker–worker relatedness is found in D. arenaria. D. arenaria is a common yellowjacket wasp of North America, forming annual colonies of up to several hundred workers. Queens (Figure 1) are facultatively polyandrous, with some queens mating with two or more males, and workers are capable of worker maleproduction [15]. In Loope’s [7] study population in New York State, USA, 42% of colonies were queenless (excluding incipient and senescing colonies). By bringing colonies into the laboratory and painstakingly filming them in observation boxes, Loope [7] observed worker matricide of the queen in three cases. In each, a single worker began to sting the queen, and in two cases this worker was joined by others in its attack. Although the queen sometimes defended herself, in all three cases only the queen died. Hence the queen should indeed lie uneasy, because her own daughters may prove to be her assassins. These observations, together with estimates suggesting that intrinsic queen mortality is
Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved R1077
Current Biology
Dispatches
Figure 1. Queen Dolichovespula arenaria wasp in the nest.
D. arenaria queens, including this marked one, risk being killed by their own worker daughters. (Photo credit: Kevin Loope.)
low, led to the inference that almost all (c. 90%) of queenlessness in mature, presenescence colonies was caused by worker matricide. Loope [7] next carried out a detailed genetic analysis using polymorphic microsatellite markers of a sample of 21 colonies collected from the field. This yielded measures of the level of worker– worker relatedness, which turned out to vary with both mating frequency and the extent to which, in offspring of polyandrous queens, the queen’s mates shared paternity (paternity skew). An analysis then revealed that worker–worker relatedness was associated with a colony’s queen status, being significantly higher in queenless than in queenright colonies (r = 0.69 v. 0.52, respectively). In short, queenlessness, the primary cause of which is worker matricide, occurred preferentially in colonies where workers would be most closely related to workerproduced males. This matched the prediction from inclusive fitness theory [6]. The conclusion that the kin structure of the colony causally affects the likelihood of worker matricide rests on ruling out plausible alternative explanations for the association of high relatedness with queenlessness. In this respect, Loope’s [7] study makes a strong case. For example, one possibility is that highrelatedness colonies contained inbred
queens likely to produce diploid males and thereby induced worker matricide. In Hymenoptera, haplodiploidy is associated with a system of sex determination in which homozygosity at a sex-determining locus, which may stem from inbreeding, creates diploid males. As these male are sterile, they represent a substantial cost to the colony [16] and workers might benefit from eliminating queens producing such males. However, in the present study, singly-mated D. arenaria queens had not inbred, ruling out this explanation [7]. Furthermore, a colony’s stage in the colony cycle, implicated in explaining differences in levels of worker male production in queenright conditions in another Dolichovespula species [17], did not explain the association found. Most tellingly, high worker–worker relatedness did not always arise from single queen mating in D. arenaria. In some colonies, it arose because polyandrous queens exhibited high paternity skew, so elevating relatedness among their worker offspring. Such skewed paternity could itself be a response to an inbred pairing between the queen and at least one of her mates [7]. Regardless, an analysis showed that, among polyandrous queens, paternity skew was significantly higher in queenless than in queenright colonies [7]. This result was as expected
if high relatedness stemming from high paternity skew induced matricide and suggested that relatedness, not mating frequency per se, underlies the association with matricide. It is also consistent with workers assessing their colony’s kin structure from chemical cues covarying with nestmate relatedness, as suggested in other eusocial insects [18], rather than directly from the queen’s mating frequency [7]. Loope’s [7] fine study breaks new ground by taking research on worker matricide firmly into the empirical realm. Although experimental confirmation of its inferences lie in the future, it provides very strong evidence for inclusive fitness theory’s predicted link between worker–worker relatedness and matricide. In so doing, it further rebuts recent criticism of the utility of the theory [19,20] and shows how cooperation, depending on context, can degenerate into conflict in ways the theory predicts. REFERENCES 1. Bourke, A.F.G. (2011). Principles of Social Evolution (Oxford: Oxford University Press). 2. West, S.A., Fisher, R.M., Gardner, A., and Kiers, E.T. (2015). Major evolutionary transitions in individuality. Proc. Natl. Acad. Sci. USA 112, 10112–10119. 3. Hamilton, W.D. (1964). The genetical evolution of social behaviour I, II. J. Theor. Biol. 7, 1–52. 4. Trivers, R.L., and Hare, H. (1976). Haplodiploidy and the evolution of the social insects. Science 191, 249–263. 5. Ratnieks, F.L.W., Foster, K.R., and Wenseleers, T. (2006). Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581–608. 6. Bourke, A.F.G. (1994). Worker matricide in social bees and wasps. J. Theor. Biol. 167, 283–292. 7. Loope, K.J. (2015). Queen killing is linked to high worker-worker relatedness in a social wasp. Curr. Biol. 25, 2976–2979. 8. Bourke, A.F.G. (1988). Worker reproduction in the higher eusocial Hymenoptera. Q. Rev. Biol. 63, 291–311. 9. Bulmer, M.G. (1983). The significance of protandry in social Hymenoptera. Am. Nat. 121, 540–551. 10. Ratnieks, F.L.W. (1988). Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217–236. 11. Foster, K.R., and Ratnieks, F.L.W. (2001). Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav. Ecol. Sociobiol. 50, 1–8.
R1078 Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved
Current Biology
Dispatches 12. Bloch, G., and Hefetz, A. (1999). Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies. Behav. Ecol. Sociobiol. 45, 125–135. 13. Strassmann, J.E., Nguyen, J.S., Are´valo, E., Cervo, R., Zacchi, F., Turillazzi, S., and Queller, D.C. (2003). Worker interests and male production in Polistes gallicus, a Mediterranean social wasp. J. Evol. Biol. 16, 254–259. 14. Soro, A., Ayasse, M., Zobel, M.U., and Paxton, R.J. (2009). Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insectes Soc. 56, 55–63.
15. Freiburger, B.J., Breed, M.D., and Metcalf, J.L. (2004). Mating frequency, within-colony relatedness and male production in a yellow jacket wasp, Dolichovespula arenaria. Mol. Ecol. 13, 3703–3707.
18. Boomsma, J.J., Nielsen, J., Sundstro¨m, L., Oldham, N.J., Tentschert, J., Petersen, H.C., and Morgan, E.D. (2003). Informational constraints on optimal sex allocation in ants. Proc. Natl. Acad. Sci. USA 100, 8799–8804.
16. Cook, J.M., and Crozier, R.H. (1995). Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10, 281–286.
19. Nowak, M.A., Tarnita, C.E., and Wilson, E.O. (2010). The evolution of eusociality. Nature 466, 1057–1062.
17. Bonckaert, W., Van Zweden, J.S., D’Ettorre, P., Billen, J., and Wenseleers, T. (2011). Colony stage and not facultative policing explains pattern of worker reproduction in the Saxon wasp. Mol. Ecol. 20, 3455–3468.
20. Abbot, P., Abe, J., Alcock, J., Alizon, S., Alpedrinha, J.A.C., Andersson, M., Andre, J.B., van Baalen, M., Balloux, F., Balshine, S., et al. (2011). Inclusive fitness theory and eusociality. Nature 471, E1–E4.
Animal Evolution: Only Rocks Can Set the Clock Davide Pisani1,2,* and Alexander G. Liu2 1School
of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK of Earth Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.10.015 2School
Molecular clocks have become the method of choice to date the tree of life. A new study demonstrates that there are limits to their precision, which may only be overcome by improving our knowledge of the fossil record. When did animals (the Metazoa) evolve [1–4]? Can we correlate the evolutionary history of animals with specific events in Earth history to understand what drove their origin and subsequent diversification [1–4]? For example, was the origin of animals triggered by the emergence of modern, well-oxygenated oceans [5], or did oxygenated oceans emerge as a consequence of the evolution of spongelike animals capable of removing dissolved carbon from the water column and sequestering it within sediments [6,7]? These and other similar questions have fascinated scientists for generations, and are united by the requirement of an accurate and precise timescale of animal evolution to answer them. Attempts to offer such a timescale often utilise methods based on the molecular clock. The molecular clock — first proposed by Emile Zuckerkandl and Linus Pauling in 1962 — works on the premise that the number of mutations independently accumulating in the genomes of living organisms is to some level proportional to the time that has elapsed since they shared a common ancestor [8]. However, a new study by dos Reis and colleagues [1]
in this issue of Current Biology demonstrates that, at present, these methods are not precise enough to correlate milestones in early animal history with events in the geological record. Scientists have long relied on fossils to draft a timescale of animal evolution, but the fossil record is beset by several rather annoying flaws. Due to the vagaries of sedimentary, tectonic and erosive processes, the fossil record is incomplete [9]. Furthermore, the oldest known fossil of a given species identifies only its first appearance in the rock record, which generally corresponds to a time when the species was already well established, with stable and abundant populations. The biological origin of a given species will always be older than its first appearance in the fossil record [10]. Finally, the deeper we delve into Earth history, the harder it becomes to recognise specific fossils as the extinct relatives of living species. DNA and proteins do not preserve well, and the genealogical relationships of fossils close to the root of the animal tree can only be defined by the presence of shared morphological features (homologies). Yet,
the further we move back in time, the smaller the number of homologies becomes [2]. As a result, whereas we can intuitively visualise the appearance of the last common ancestor of, say, humans and chimps, an animal that lived 6.5– 10 million years ago [10], picturing the last common ancestor of humans and sea cucumbers (an animal that inhabited the Earth’s oceans at least 515.5 million years ago [1–4,10]) is rather more speculative. Even experts, when faced with the fossil remains of the very first animals, struggle to confidently identify them as such, simply because they have no clear idea of what these animals were supposed to look like. Such uncertainties have shrouded the earliest history of animals in mystery. Currently, the best candidates for the oldest possible animal fossils are members of the diverse and largely softbodied Ediacaran macrobiota, found in rocks dated to 580–541 million years ago [11]. However, many of these organisms have proven difficult to interpret, with little agreement as to whether iconic taxa such as Dickinsonia, Fractofusus, or Spriggina (Figure 1) are
Current Biology 25, R1070–R1091, November 16, 2015 ª2015 Elsevier Ltd All rights reserved R1079