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(BQ) Part 1 book Orinciples of animal behavior has contents: Principles of animal behavior, the evolution of behavior, hormones and neurobiology, molecular genetics and development, learning, cultural transmission, sexual selection, mating systems.
PRINCIPLES OF ANIMAL BEHAVIOR THIRD EDITION Lee Alan Dugatkin Principles of Animal Behavior THIRD EDITION Principles of Animal Behavior THIRD EDITION Lee Alan Dugatkin UNIVER SIT Y OF LOUIS VILLE B W W NORTON & COMPANY | NE W YORK | LONDON W W Norton & Company has been independent since its founding in 1923, when William Warder Norton and Mary D Herter Norton first published lectures delivered at the People’s Institute, the adult education division of New York City’s Cooper Union The firm soon expanded its program beyond the Institute, publishing books by celebrated academics from America and abroad By midcentury, the two major pillars of Norton’s publishing program—trade books and college texts—were firmly established In the 1950s, the Norton family transferred control of the company to its employees, and today—with a staff of four hundred and a comparable number of trade, college, and professional titles published each year—W W Norton & Company stands as the largest and oldest publishing house owned wholly by its employees Editor: Betsy Twitchell Development Editor: Beth Ammerman Project Editor: Amy Weintraub Electronic Media Editor: Carson Russell Editorial Assistant: Courtney Shaw Marketing Manager, Biology: John Kresse Production Manager: Eric Pier-Hocking Photo Editor: Stephanie Romeo Permissions Manager: Megan Jackson Book Design: Leelo Märjamaa-Reintal / Rubina Yeh Design Director: Rubina Yeh Composition: TSI Graphics Manufacturing: Courier Kendallville The text of this book is composed in Fairfield LT with the display set in Meta Plus Copyright © 2014, 2009, 2004 by W W Norton & Company, Inc All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Dugatkin, Lee Alan, 1962Principles of animal behavior / Lee Alan Dugatkin Third edition pages cm Includes bibliographical references and index ISBN 978-0-393-92045-1 (pbk.) Animal behavior I Title QL751.D748 2013 591.5 dc23 2013004071 W W Norton & Company, Inc., 500 Fifth Avenue, New York, NY 10110-0017 wwnorton.com W W Norton & Company Ltd., Castle House, 75/76 Wells Street, London W1T 3QT For Jerram L Brown, my mentor and friend Contents in Brief 10 11 12 13 14 15 16 17 Principles of Animal Behavior The Evolution of Behavior Hormones and Neurobiology Molecular Genetics and Development Learning Cultural Transmission Sexual Selection Mating Systems Kinship Cooperation Foraging Antipredator Behavior Communication Habitat Selection, Territoriality, and Migration Aggression Play Animal Personalities 28 68 104 128 164 198 236 270 306 346 382 416 448 480 510 538 V II equal fitness (Krebs and Davies, 1987) It is this equivalency of fitness among monogamous and polygamous females that makes the PTM stable Because monogamous females and females in polygamous relationships settle in such a way as to produce approximately equal fitness, there is no temptation for females to move from territory to territory once this state has been reached, as any such move would in fact lower an individual’s reproductive success (see BorgerhoffMulder, 1990, for some limitations of the PTM) THE P TM AND M ATE CHOICE IN F EM ALE BIRDS Wanda Pleszczynska used lark buntings (Calamospiza melanocorys) in one of the first experimental tests of the PTM In lark buntings, the resource that primarily determines female settlement onto male territories is shade cover, as the main cause of nestling mortality in lark buntings is overheating The more shade on a territory, the better the territory, and this shade effect can be shown experimentally by artificially increasing the shade in a given territory, which leads to an increase in nestling survival (Pleszczynska and Hansell, 1980) Because shade protection is such a critical resource, it will often be the case that the male territories that are best suited to provide shade have already been settled by other females (Figure 8.17) Settling on a territory in which there already is a male and a female and becoming a “secondary” female allows a female access to shading The cost of becoming such a secondary female is that a male only provides paternal care to the nestlings of his “primary” female, the mate that arrived first (Krebs and Davies, 1987) Pleszczynska and Hansell found that increasing shade availability on a territory not only made it much more sought after by females, but that as the PTM predicts, secondary females that bred in areas with shade cover (but that did not receive male aid) had about the same reproductive success as did monogamous females that bred on territories with less shade cover (but that did receive male aid) Territory (more shade) Male Territory (less shade) Female Female ? ? Male Female FIGURE 8.17 The polygyny threshold model In the lark bunting, shade is a limiting resource, as it affects nestling survival Females may choose the territory of a male with good shade cover (territory 1) over a territory with less shade cover (territory 2), even if this decision means entering a polygynous relationship rather than a monogamous one T H E E CO L O G Y A N D E V O L U T I O N O F P O LY G Y N O U S M AT I N G S Y S T E M S | 55 EXTR APAIR COPULATIONS FIGURE 8.18 Indigo buntings (A) A female indigo bunting Although socially monogamous, female indigo buntings are often involved in extrapair copulations (B) A male indigo bunting Males defend their territories against intruders (Photo credits: David Westneat) A 256 | C H A P T E R | M AT I N G S Y S T E M S Male and female birds often form pair bonds at their nest during breeding season It was once thought that such pairings were monogamous, in the sense that members of a given pair only mated with their nesting partner during a breeding season Starting in the early 1980s, however, ornithologists began to uncover more and more instances of what are now referred to as extrapair copulations, or EPCs (R Ford and McLauglin, 1983; McKinney et al., 1984) Ethologists were finding that males and females were leaving their territories during the mating season and mating with other individuals, usually those in nearby territories The occurrence of such EPCs prompted some animal behaviorists to make a distinction between social monogamy and genetic monogamy Most bird species in which EPCs were recorded formed pair bonds with just a single partner during a mating season, and as such displayed what is referred to as social pair bonding, or social monogamy Yet, genetically, these systems resembled promiscuity more than monogamy, as mating occurred both with the social partner and with other individuals during the mating season The increased reproductive success of males that leave territories and engage in EPCs seems clear, as they can fertilize more females But why would a female be involved in EPCs? The answer depends on the particular species and its ecology and demographics, but in general, females engaging in EPCs may (1) increase the probability that all their eggs are fertilized (the fertility insurance hypothesis); (2) maximize genetic diversity in their offspring, thereby increasing the chances that some of the offspring fare well in the environment in which they mature (Blomqvist et al., 2002, 2003; Griffith and Montgomerie, 2003); (3) use EPCs to select males that have good genes (see Chapter 7) but that might not be willing to form a pair bond and provide direct benefits to their offspring (Griffith et al., 2002; Neudorf, 2004); and (4) increase the amount of direct benefits—food, protection, and so on—that they receive from males David Westneat was among the first researchers to uncover the extent to which EPCs are occurring in nature His behavioral observations of indigo buntings suggested that about 13 percent of all matings were EPCs (Westneat, 1987b; Figure 8.18) Westneat was concerned, however, that such observations might underestimate the actual percentage of all offspring that were sired via extrapair copulations Because buntings were hard to follow for long periods at B a time, a significant number of EPCs may have been missed Furthermore, it was not clear how many extrapair matings translated into extrapair fertilizations For example, indigo bunting females generally resisted EPCs to a greater extent than mating with their nesting partner: Females resisted EPCs in 34 out of 43 attempts, but only resisted mating with their pairmates in 72 out of 320 attempts (Westneat et al., 1987) Not all EPCs result in offspring To examine what impact EPCs had on mating dynamics in buntings, Westneat ran a genetic analyses of parentage done in conjunction with a detailed behavioral study (Westneat, 1987a; Figure 8.19) This study was conducted before DNA fingerprinting techniques were widely available, and it relied on a technique called electrophoresis, which, although less powerful than DNA fingerprinting, does allow ruling out a particular adult individual as the parent of a particular offspring Over the course of two years, Westneat obtained DNA samples from hundreds of individually recognizable buntings Using electrophoretic comparisons, and plugging that data into existing mathematical models, he found that, of the 257 young that were examined, 37 had genotypes that were not consistent with the genotype of one of their presumed parents (Westneat, 1987a), so at least 14 percent (37 out of 257) of all young were sired via an extrapair copulation— right in line with the 13 percent Westneat had predicted based on his behavioral observations After that analysis, however, updated mathematical models showed that electrophoretic estimates of the percentage of young fathered by extrapair fertilizations in buntings were underestimates Plugging Westneat’s numbers into these newer models uncovered extrapair fertilization rates between 27 to 42 percent (depending on the year) in buntings (Westneat et al., 1987) Since Westneat’s work, many studies have documented EPC frequency in birds (for example, Adler, 2010; C E Hill et al., 2011; Schmoll, 2011), and have found that EPCs account for 76 percent of all young in one population of the superb fairy wren (Malurus cyaneus; Mulder et al., 1994; M S Webster Both extrapair copulations and within-pair copulations are highest at day before egg laying A B Copulations/hours pair was observed Copulations/hours female was observed 5.0 4.0 3.0 2.0 1.0 2.5 2.0 1.5 1.0 0.5 12–8 Number of days before egg laying –1 12 –8 Number of days before egg laying –1 FIGURE 8.19 Copulations in indigo buntings Occurance of copulations in (A) extrapair and (B) within-pair matings The day the egg was laid is shown as day on the x-axis (Based on Westneat, 1987b) T H E E CO L O G Y A N D E V O L U T I O N O F P O LY G Y N O U S M AT I N G S Y S T E M S | 57 and Westneat, 1998; Westneat et al., 1990) Given that monogamy was long considered to be the norm in birds, these are staggering numbers—numbers that are available only because of the revolution in molecular genetics that is still underway today SPERM COMPETITION In many polyandrous and promiscuous breeding systems, there is a great deal of variation in reproductive success between individuals With respect to males, a few individuals may obtain the vast majority of matings in a population, and many males may fail to obtain even a single mating opportunity In Chapter 7, we saw how both male-male competition and female mate choice can affect which males are on the upper and lower ends of this mating curve distribution Here, we will look at the effect of sperm competition—that is, the direct competition between the sperm of different males to fertilize a female’s eggs—on mating success and the evolution of mating systems (Birkhead and Møller, 1992, 1998; Birkhead and Parker, 1997; G A Parker and Pizzari, 2010; Tourmente et al., 2011) In some promiscuous (as well as some polyandrous) mating systems, males compete not only for access to mating opportunities with females, but directly for access to eggs In these systems, competition also occurs after a female has mated with numerous males If females store sperm from numerous matings, sperm from different males may compete with one another over access to fertilizable eggs (Figure 8.20) When sperm competition exists, selection can operate directly on various attributes of sperm, such as sperm size and shape Mature ovum Immature ovum Sperm storage tubules in uterovaginal junction Oviduct Domestic fowl (hen) Uterus (shell gland) Cloaca FIGURE 8.20 Sperm competition The reproductive system of domestic fowl Sperm storage occurs in sperm storage tubules (SST) at the uterovaginal junction Females in many species can store sperm from multiple males, setting the stage for sperm competition Only a small proportion of sperm makes it into the SST (Based on Birkhead and Møller, 1992) 258 | C H A P T E R | M AT I N G S Y S T E M S SPERM COMPETITION IN DUNGFLIES Sperm competition has been extensively documented in many groups of animals, and a similar sort of competition, known as “pollen competition,” is known to occur in plants (Delph and Havens, 1998) One of the leaders in this field, in terms of both empirical and theoretical aspects of sperm competition, is Geoff Parker, whose initial work on sperm competition in dungflies is regarded as the origins of modern research in this area (Immler et al., 2011; G. Parker, 1970b, 2001; G A Parker and Pizzari, 2010) Dungflies use the droppings of large, often domestic, animals for breeding sites While in most insects, copulations often last a matter of seconds, in dungflies they can last on the order of thirty minutes or more After a detailed analysis of the natural history of mating in dungflies in pastures, Parker was faced with a number of unresolved issues regarding dungfly mating When a new dung pat is created and females begin to arrive, there ensues intense male competition for mating opportunities A thousand or so males can descend on a single dung pat, all in search of females Males that find a female and begin copulating are under constant physical attack from other males trying to break up their pairing and start their own round of copulating (Figure 8.21) To test for the role of sperm competition in this mating system, Parker relied on a technique that entomologists of the day had been using in various biocontrol programs (G Parker, 1970a) He irradiated the sperm of certain males, creating males whose sperm would then fail to produce eggs that hatched As such, Parker could take pairs of males, irradiate one of them, and then examine the relative success of each male by simply determining the proportion of eggs that failed to hatch—that is, the proportion of fertilizations attributable to the irradiated male A B A male passively guards a female against other males Dungflies copulating C D A male struggles with an intruder attempting to displace him A male actively guards a female from another male FIGURE 8.21 Dungfly mating In dungflies, sperm competition can be intense, with the last male copulating with a female fathering up to 80 percent of her offspring (Photo credits: Geoff Parker) T H E E CO L O G Y A N D E V O L U T I O N O F P O LY G Y N O U S M AT I N G S Y S T E M S | 59 Parker found that the number of eggs that were fertilized by the last male to mate with a female was proportional to how long such a mating lasted The longer the last mating, the greater the reproductive success of the male More specifically, the longer such a copulation, the greater the extent to which the last male’s sperm displaced the sperm of males that had copulated with the female earlier (Figure 8.22) Such “last male precedence” is common when sperm competition is in play, but it is not ubiquitous (In some mating systems, sperm competition appears to favor the first, rather than the last, male to mate with a female.) In the dungfly system, the last male to mate with a female copulated on average for thirty-six minutes, and as a result he fathered approximately 80 percent of the young in the clutch of eggs deposited by a female (G. Parker, 1970a) If copulation time correlates with greater displacement of a competitor’s sperm, why don’t males copulate for even longer periods and thereby attempt to displace 100 percent of a competitor’s sperm? The answer appears to be that males must weigh such an option against what else could be done with the time in question While increasing the time spent with female A will increase the displacement effect, it is also time that the male could have used to find another female with whom to mate Because the rate of sperm precedence slows down with time, it will often benefit a male to use such additional time to find other potential mates (G A Parker, 1974b; G A Parker and Stuart, 1976) SPERM COMPE TITION IN SE A URCHINS While sperm competition is often thought of in terms of its effect in utero, it can also play an important role in species that not have internal fertilization To get a better sense of the importance of sperm competition in such systems, let’s consider Don Levitan’s work on sperm velocity and fertilization rates in the sea urchin (Levitan, 2000) Levitan began his work by hypothesizing that variation in the speed at which sperm traveled correlated with fertilization rate Using sea urchin sperm makes this task a bit easier than using sperm from birds or mammals, because sea urchins secrete their sperm and eggs into seawater With a video camera that can tape sperm swimming along and a microscope to see which eggs Proportion of fertilizations 1.0 0.8 0.6 0.4 0.2 0.0 Copulation duration of second male (minutes) 10 FIGURE 8.22 Sperm competition in dungflies The longer a male dungfly mates with a female dungfly, the greater his fertilization success (From Simmons, 2001) 260 | C H A P T E R | M AT I N G S Y S T E M S are fertilized, Levitan was able to measure the sperm’s swimming speed and fertilization success Levitan found that to fertilize the same number of eggs, males that produced slow-moving sperm needed to release up to 100 times more sperm than males that produced fast-moving sperm (Figure 8.23) Levitan then examined what happens to sperm as they age In so doing, he was examining a predicted trade-off between the speed at which a sperm moves and how long that sperm survives Because swimming fast and swimming for a long time both require energy, fast-moving sperm shouldn’t live as long as slow-moving sperm When examining the expected trade-off between speed and longevity, Levitan first found that all sperm slow down as they get older (Figure 8.24) Not only did sperm decrease their swimming speed with age, but as they aged, they were much less likely to fertilize an egg, even when they encountered one For example, sperm that were only an hour old could be up to 100 times less likely to fertilize an egg as were newly released sperm After two hours, sperm fertilized no eggs at all With data on longevity and speed in hand, Levitan could return to the question raised earlier: Is there a trade-off between sperm speed and sperm life span for individual sea urchins? The answer appears to be yes, as Levitan found a negative correlation between velocity and endurance Individuals that produced fast-moving sperm had their sperm become ineffective at much quicker rates than other individuals The energy used up in swimming fast resulted in less energy for swimming for a long time, as well as a shorter life span for sperm Number of sperm per microliter needed to fertilize 50% of female’s eggs 0.1 0.2 0.3 Sperm velocity (mm/s–1) FIGURE 8.23 Sperm velocity and fertilization In sea urchins, slower sperm fare poorly The slower the sperm, the more sperm needed to fertilize a female’s eggs (Based on Levitan, 2000) OTHER EFFEC TS OF SPERM COMPE TITION Sperm competition not only affects the speed at which sperm swim but also affects the various shapes and functions that sperm can take (Bellis et al., 1990; Gomendio et al., 1998; Holman and Snook, 2006; H Moore et al., 1999, Tourmente et al., 2011) For example, Roger Baker and Mike Bellis’s kamikaze sperm hypothesis suggests that natural selection might favor the production of some sperm types that are A B Number of sperm per micr0liter needed to fertilize 50% of a female’s eggs Mean velocity (mm/s–1) 0.300 0.200 0.100 30 60 90 120 Sperm age (minutes) 20 40 60 Sperm age (minutes) FIGURE 8.24 Older sperm fare poorly (A) In sea urchins, older sperm swim slower, and (B) a greater quantity of such sperm is needed to achieve high fertilization rates (Based on Levitan, 2000) T H E E CO L O G Y A N D E V O L U T I O N O F P O LY G Y N O U S M AT I N G S Y S T E M S | 61 designed to kill other males’ sperm rather than fertilize eggs (Baker and Bellis, 1988) While the evidence is equivocal in humans, sperm competition has had clear effects on sperm morphology in insects, frogs, mammals, birds, fish, and worms (Baer et al., 2009; Birkhead and Møller 1992, 1998; Eberhard, 1996; Firman and Simmons, 2010; Stockley et al., 1997; Tourmente et al., 2009, 2011; Figure 8.25) For example, in a phylogenetic analysis of 100 species of Australian (myobatrachid) frogs, Philip Byrne and his colleagues found that males in species with intense sperm competition produced sperm with relatively long tails (P. G Byrne et al., 2003) While the exact advantage of longer-tailed sperm in these frogs is not yet known, other studies have found that sperm with longer tails swim faster than their shorter-tailed competitors, and hence have an increased probability of fertilizing an ovum (Oppliger et al., 2003) Sperm competition also has effects on the number of sperm produced per ejaculate One prediction from sperm competition theory is that the number of sperm per ejaculate should be a function of the probability that a female has recently mated with other males (Baker and Bellis, 1993) To see this, consider two males that we will call M1 and M2 Suppose that M1 is about to copulate with a female The greater the chance that such a female has mated with M2 in the recent past and that his sperm are still present, the greater the chance that M1’s and M2’s sperm will be in direct competition to fertilize the eggs of the female Under this scenario, sperm competition theory predicts that M1 will ejaculate more sperm in an attempt to increase the chances that he will fertilize the female’s eggs Baker and Bellis tested this hypothesis in humans They obtained data on the interval between copulations in a given pair of individuals, and assumed that the longer this interval, the greater the chances that a partner would have had a sexual encounter with someone besides their partner Then they obtained A Eosentonon transitorium D Dung beetle, Onthophagus taurus B Telmatoscopus albipuntus E Plodia interpunctella G Fruit fly, Drosophila bifurca H Tessellana tesselata C Fishfly, Parachauliodes japonicus F Water beetle, Dytiscus marginalis FIGURE 8.25 Variability in sperm morphology Sperm competition is one of the many forces that have led to incredible variability in insect sperm morphology Pictured here are (A) sperm from Eosentonon transitorium, (B) fishlike sperm from Telmatoscopus albipuntus, (C) sperm bundle from the fishfly Parachauliodes japonicus, (D) mm sperm from the dung beetle Onthophagus taurus, (E) short and long sperm from Plodia interpunctella, (F) paired sperm from the water beetle Dytiscus marginalis, (G) giant 58 mm sperm from Drosophila bifurca, and (H) hook-headed sperm from Tessellana tesselata (Based on Simmons, 2001) 262 | C H A P T E R | M AT I N G S Y S T E M S Residual number of sperm (millions) 600 400 200 –200 ≤24 73–120 121–168 168 25–72 Time since last within-pair copulation (hours) FIGURE 8.26 Sperm number in humans In humans, the number of sperm ejaculated during a copulation is a function of the time since a pair last copulated Note that the y-axis is a measure of “residuals”; hence negative values are possible (Based on Baker and Bellis, 1993) sperm samples from individuals the next time they copulated with their partner Baker and Bellis found that not only did sperm number increase as a function of time since last copulation (which could be due to many different factors), but that even when absolute time was statistically removed from the equation, the relative amount of time couples spent together predicted sperm volume as well (Figure 8.26) When couples spent more time together, and hence the risk of extrapair copulations was low, sperm count was significantly lower than when couples spent less time together With respect to sperm competition, it is important to keep in mind that females are not simply “inert environments” that serve as receptacles of male sperm (G Parker, 1970b) Rather, females themselves may play an active role in sperm competition via cryptic mate choice—that is, female mate-choice behavior that is not obvious to males William Eberhard, for example, suggests that, among other things, cryptic choice may affect how much sperm a female allows a copulating male to inseminate her with, how she goes about transferring such sperm to the organs where sperm are stored, and which sperm she may select for actual fertilization (Eberhard, 1996) Precisely how females select among sperm remains unknown in most cases, but this is an active area of study within animal behavior research (Birkhead and Pizzari, 2002; Holman and Snook, 2006) Multiple Mating Systems in a Single Population? In the case of dunnocks, which we discussed earlier in the chapter, we see monogamous, polygynous, polyandrous, and polygynandrous mating groups all in the same population Let’s return to this mating system, and examine it in a bit more detail Nick Davies and his colleagues have an ongoing, long-term study on a population of about eighty dunnocks that reside in the Botanical Gardens of M U LT I P L E M AT I N G S Y S T E M S I N A S I N G L E P O P U L AT I O N ? | INTERVIEW WITH Dr Nick Davies The dunnocks you work with have proved to be a model system for so many questions in behavioral ecology and animal behavior Why did you choose to work with this species? In 1979, when I started as a young university lecturer at Cambridge, I was excited by the new theoretical ideas of Bill Hamilton, Robert Trivers, John Maynard Smith, and Geoff Parker They were beginning to explore the evolutionary consequences of individual conflicts of interest, not only the long-recognized conflicts among rival males but also those between the male and female of a breeding pair and between parents and their offspring These ideas led to a profound change in how we interpret individual adaptations For example, the classical work on clutch size (pioneered by David Lack) had considered what would be optimal from a pair’s point of view Once genetic conflicts within families were recognized, a whole new world of possibilities was opened up, involving deception, manipulation, cheating, and compromise Likewise, previous studies of mating systems had emphasized ecological pressures (food, nest sites, predation) that might lead to one system rather than another But now we began to consider social conflicts as important selection pressures too So I was on the lookout for a field study which would allow me to take a fresh look at bird mating systems While wandering in the University Botanic Garden, I noticed the dunnocks chasing around the bushes in pairs, threes, and fours 264 | C H A P T E R | M AT I N G S Y S T E M S and decided to color-band them for individual recognition to see what was going on Once I had this initial excuse to begin the study, I then discovered more interesting new questions from the bird watching rather than from the theoretical literature Your work on the dunnock suggests these birds have an incredibly plastic mating system Why you think that is? It is clear from watching behavior that males and females have different mating preferences These conflicts make good sense in relation to individual reproductive payoffs from the different mating combinations For a female, polygyny (one male plus two females) was the least successful option, because she had to share the help of one male with another female, and her chicks often starved In polygyny, females often chased and fought each other If one of them could drive the other away, then she could claim the male’s fulltime help and so enjoy the greater success of monogamy A polyandrous female (one female with two males) was even more successful: if she shared copulations between both her males, then both helped to feed her brood With this extra help, more chicks survived This explained why a female encouraged both alpha and beta males to copulate with her Our experiments showed that she maximized total male help by sharing copulations equally between the two males By contrast, a male fared least well in polyandry Although more young were raised, there was the cost of shared paternity Our DNA fingerprinting results showed that an alpha male did better with full paternity of a pair-fed brood This explains why alpha males acted against the female’s wishes, and tried to drive beta males away, or at least prevent them from copulating A male did best of all in polygyny, the system in which a female did worst Although each female was less productive, the combined output of two females in polygyny exceeded that of a monogamous female So once again there was conflict—the male intervened in the squabbles between his two females in an attempt to retain them both The variable mating system thus reflects the different outcomes of sexual conflict Where a male can prevent the conflicts between two females, we find polygyny Where a female can escape the close guarding of her alpha male, and give a mating share to the beta male, we observe polyandry Monogamy occurs when neither sex can gain a second mate Polygynandry—for example, two males with two females—can be viewed as a “stalemate”: the alpha male is unable to drive the beta male off and so claim both females for himself, and neither female can evict the other and so claim both males for herself So the interesting question is What determines whether particular individuals can get their best option despite the conflicting preferences of others? This is influenced by individual competitive ability and various practical considerations, such as vegetation density (which determines how easily an alpha male can follow a female) The main point is that the social conflicts are played on an ecological stage, which may affect the likely outcomes Sexual selection and mating systems are often presented as two distinct topics Is it possible to understand one without the other? Darwin’s theory of sexual selection aims to explain the evolution of traits that increase an individual’s mating success: size, weapons, ornaments, mate choice, and so on Mating systems are the outcomes of this competition for mates So you need to think about both process and outcome for a full understanding Why you think polyandry is rare compared to polygyny? When you look at social groups, it is certainly true that you more often see one male defending a group of females rather than the converse— namely, one female defending a group of males In theory, this is exactly what you would expect, because a male usually has a greater potential reproductive rate than a female This means that an increase in the number of mates leads to a much greater increase in male reproductive success than it does in female reproductive success Thus, males often go for quantity, while females seek quality, when they search for mates Nevertheless, until recent years we underestimated the frequency with which females seek matings with multiple males They often this surreptitiously, sometimes outside their social groups, to increase their access to resources, to increase male care, to reduce male harassment, or to improve the genetic quality of their offspring Males often go for quantity, while females seek quality, when they search for mates Nevertheless, until recent years, we underestimated the frequency with which females seek matings with multiple males They often this surreptitiously There has been some debate as to who calls the shots when it comes to mating systems—males or females? Clearly any given mating requires both a male and female, but are there certain situations in which you expect males to be controlling the mating system, and others where mating systems are primarily under the control of females? Darwin’s theory of sexual selection aimed to explain how individuals competed for mates He proposed two processes: people readily accepted the first, namely, male-male competition (Darwin’s “law of battle”), but were reluctant to believe the second, namely, female choice We now have good evidence for this, of course It is interesting to see reactions to Parker’s theory of sperm competition (sexual selection after the act of mating) follow the same history At first, everyone focused on males—mate guarding, frequent copulation, mating plugs, sperm removal, testis size, and so on Consideration of female roles (“cryptic female choice” of sperm) came later, and it is still controversial My guess is that female roles will be crucial, simply because females should be better able to control events inside their own bodies In some cases, the act of mating seems to be under male control; for example, where female insects lay their eggs in localized patches (e.g., cow pats), powerful males can monopolize the laying sites, and a female is forced to mate in order to gain access In other cases, females can more easily escape males; for example, insects that lay their eggs in more dispersed sites can often refuse matings, and in birds (where females can often easily escape males by flying off) mating rarely occurs without female consent It will be interesting to see whether cryptic female choice of sperm is more likely in cases where females have less control over the act of mating Dr Nick Davies is a professor at Cambridge University in England His long-term work on dunnocks, summarized in Dunnock Behaviour and Social Evolution (Oxford University Press, 1992), elegantly shows the complexity of animal mating systems and how one goes about testing fundamentally important hypotheses in such a system I N T E R V I E W W I T H D R N I C K D AV I E S | 65 Cambridge University, and their work has provided a rare detailed portal into a complex mating system (Davies, 1992) What makes the dunnock breeding biology so fascinating from a mating systems perspective is the long-term persistence of monogamy, polygyny, polyandry, and polygynandry in the same population For Davies, unraveling the story behind the dunnock mating system is akin to detective work: “The puzzle is the dunnock’s extraordinary breeding behavior and variable mating system The job of the nature detective is to understand alternative options facing individuals, to assess their reproductive payoffs, and then to discover whether different mating strategies might emerge as a result of individuals competing to maximize their reproductive success” (Davies, 1992, p 21) Underlying much of the variance in mating systems, including that of the dunnock, is the fact that the fitness of males and females is affected in different ways by the mating system Reproductive success of the most successful males will often be lowest when they share access with other males to a single female (polyandry), and then increase in the following order: sole access to a single female (monogamy), joint access to two females (polygynandry), and sole access to numerous females (polygyny) In other words, male reproductive success increases as a function of both the number of mates and the degree to which a male has sole reproductive access to such mates The reproductive success of the most successful females increases in precisely the opposite direction, with polyandrous and polygynandrous females having the highest reproductive success As such, a conflict of interest between the sexes—sometimes referred to as a “battle of the sexes”—exists with respect to what constitutes the optimal breeding system (Arnqvist and Rowe, 2005; Hosken et al., 2009) In dunnocks, females appear to be winning this battle of the sexes (at least for now), as over the course of ten years, 75 percent of females and 68 percent of males observed by Davies and his team were involved in either polyandrous or polygynandrous mating groups (Davies, 1992) The battle of the sexes, in conjunction with the dispersal patterns of dunnocks, helps us better understand the complex breeding system found in this bird Early in the breeding season, females compete with one another to establish territories, and such female territories are chosen independently of the position of males Males then attempt to build their own territories so that they overlay as many female territories as possible Given these conditions, Davies argues that the difference between monogamy and polygyny is a function of male territory size Polygynous males had larger territories than monogamous males, but when these two breeding systems were compared, the territory size of females remained constant In contrast, the difference between polyandry and polygynandry was a function of female territory size Male territory size remained constant across these systems, while female territory size was significantly larger in the former Because all individuals in this population were marked (with color rings) and rarely moved more than two miles from the Botanical Gardens, Davies was able to undertake experiments designed to gauge more precisely how resource defense and territoriality influenced the dunnock mating system Davies and Arne Lundberg hypothesized that because females were in strong competition with one another for territories with the best resources, if the resources available on a territory were experimentally supplemented, territory size should shrink, as females would then be able to obtain the same amount of resources without having to defend as large an area (Davies and Lundberg, 1984) 266 | C H A P T E R | M AT I N G S Y S T E M S TABLE 8.2 Food and territory size Supplementing the food on dunnock territories led to a decrease in female territory size but not male territory size (From Davies, 1992, p 63) TERRITORY SIZE (m 2) WITH FEEDER CONTROL SIGNIFICANCE Females MEAN (SE) n MEAN (SE) n OF DIFFERENCE 2,776 (379) 28 4,572 (456) 39 2,864 (340) 11 2,642 (416) 13 NS 5,276 (797) 14 6,614 (674) 17 NS P < 0.01 Males Territory defended by one male Territory defended by two males To test their hypothesis, Davies and Lundberg placed artificial feeders on a randomly selected set of female territories, and they did indeed find that the female territories shrank as predicted Moreover, they found that the male territories that overlay the manipulated female territories did not change in size (Table 8.2) What did occur, however, was a shift in the distribution of mating systems, in such a manner as to favor males When female territory size shrank as a result of supplemental resources, males were better able to monopolize more than one female, and a shift away from polyandry and toward polygynandry occurred This finding supports Davies’s argument that, in the dunnock, females track resources, males track females, and the resulting interaction helps us better understand the incredible variation in mating systems in this small brown bird SUMMARY Animal mating systems are classified as monogamous, polygynous, polyandrous, polygynandrous, or promiscuous, depending on the number of mates that males and females take and the timing of such mating in relation to breeding season A female can often fertilize all her available eggs by mating with one or a very few males, so female fecundity is not so much tied to the availability of mates as it is to the availability of resources, such as food, defense, and so on Up to a point, the more resources available, the more offspring females can produce Males can potentially fertilize many females, so their reproductive success is tied more to access to females than to access to resources Male dispersion patterns should track the dispersion of females Recent work in neurobiology and endocrinology has provided animal behaviorists with a better understanding of the proximate underpinnings of both monogamy and polygamy Phylogenetic work has shed light on the relationship between mating systems and habitat quality Monogamous systems are often found in poor habitats, and polygynous systems are found in better habitats S U M M A R Y | 67 The polygyny threshold model predicts under what conditions polygyny should occur in nature In this model, females weigh the costs and benefits associated with being in a polygynous relationship on a good territory versus a monogamous (or more precisely, a less polygynous) relationship on a poorer territory While extrapair copulations and extrapair matings were once thought to be rare in birds, genetic evidence suggests that this is far from the case in many species In some mating systems, males compete not only for access to mates but directly for access to eggs If females store sperm from numerous matings, sperm from different males compete with one another over access to fertilizable eggs in what is known as sperm competition DISCUSSION QUESTIONS Define and distinguish among serial monogamy, serial polygyny, simultaneous polygyny, promiscuity with pair bonds, and promiscuity without pair bonds Read Jenni and Colliers’s 1972 article “Polyandry in the American Jacana (Jacana spinosa)” in Auk (vol 89, pp 743–765) What selective forces favored polyandry in jacanas? Why you think that polygamous mating systems more strongly favor the evolution of virulent diseases in animals and humans than monogamous breeding systems? Think about this from the perspective of the diseasecausing agent Define an EPC How does this differ from an extrapair mating? Why did it take ethologists so long to recognize the extent of EPCs in nature? How has molecular genetics revolutionized the way we think of mating systems in birds? How has natural selection via sperm competition shaped both sperm morphology and male behavior? Create a list of potential ways in which females may affect sperm competition and its outcome What is a lek, and why is that form of polygyny especially interesting to ethologists? How has knowledge of kinship bonds contributed to an understanding of why males form leks? SUGGESTED READING Arnqvist, G., & Rowe, L (2005) Sexual conflict Princeton, NJ: Princeton University Press A book-length treatment of sexual conflict and the way that it shapes mating systems Davies, N B (1992) Dunnock behaviour and social evolution Oxford: Oxford University Press A delightful book about Davies’s long-term work on dunnock behavior, with an emphasis on dunnock mating behavior Lane, J E., Forrest, M N K., & Willis, C K R (2011) Anthropogenic influences on natural animal mating systems Animal Behaviour, 81, 909– 917 An overview of how four anthropogenic factors may affect animal mating systems 268 | C H A P T E R | M AT I N G S Y S T E M S Orians, G (1969) On the evolution of mating systems in birds and mammals American Naturalist, 103, 589–603 This is the paper in which Orians presents the polygyny threshold model Parker, G (1970a) Sperm competition and its evolutionary consequences in insects Biological Reviews of the Cambridge Philosophical Society, 45, 525– 567 The seminal paper (no pun intended) of sperm competition and animal behavior Shuster, S M (2009) Sexual selection and mating systems Proceedings of the National Academy of Sciences, U.S.A., 106, 10009–10016 A review of mating systems in a special issue devoted to the 150th anniversary of the publication of Darwin’s On the Origin of Species SUGGE STED RE ADING | 269 ... 75/76 Wells Street, London W1T 3QT For Jerram L Brown, my mentor and friend Contents in Brief 10 11 12 13 14 15 16 17 Principles of Animal Behavior The Evolution of Behavior Hormones and Neurobiology... and Honeybee Foraging 11 2 Ultraviolet Vision in Birds 11 4 Song Acquisition in Birds 11 5 avpr1a, Vasopressin, and Sociality in Voles 11 8 Development and Animal Behavior 11 9 Development, Temperature,... index ISBN 978-0-393-92045 -1 (pbk.) Animal behavior I Title QL7 51. D748 2 013 5 91. 5 dc23 2 013 0040 71 W W Norton & Company, Inc., 500 Fifth Avenue, New York, NY 10 110 -0 017 wwnorton.com W W Norton