Animal Behaviour Advantages Disadvantages No2

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.2

Kevin Brewer ISBN: 978-1-904542-47-6

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6 2

This document is produced under two principles: 1. All work is sourced to the original authors. The images are all available in the public domain (most from http://commons.wikimedia.org/wiki/Main_Page ). You are free to use this document, but, please, quote the s ource (Kevin Brewer 2008) and do not claim it as you own work. This work is licensed under the Creative Commons Attribution (by) 3.0 License. To view a copy of thi s license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ or, send a letter to Creative Commons, 171 2nd Street, Suite 300, San Francisco, California, 9 4105, USA. 2. Details of the author are included so that the l evel of expertise of the writer can be assessed. This co mpares to documents which are not named and it is not poss ible to tell if the writer has any knowledge about their subject. Kevin Brewer BSocSc, MSc ( http://kmbpsychology.jottit.com/ ) An independent academic psychologist, based in Engl and, who has written extensively on different areas of psychology with an emphasis on the critical stance towards traditional ideas. Orsett Psychological Services, PO Box 179, Grays, Essex RM16 3EW UK [email protected]


CONTENTS Page Number 1. Advantages and Disadvantages of Inbreeding 4 2. Advantages and Disadvantages of Monogamy 19 3. Advantages and Disadvantages of Parental Care and Investment 35 4. Advantages and Disadvantages of Lek Mating 43 5. Advantages and Disadvantages of Non-Reproductive Sex in Animals 48


1. ADVANTAGES AND DISADVANTAGES OF INBREEDING 1.1. Introduction 1.2. Avoiding inbreeding 1.3. Adaptations with inbreeding 1.4. Amur leopards 1.5. References 1.1. INTRODUCTION Inbreeding refers to matings among genetic rel atives that reduces the variety of genes (an increase of homozygosity). "This could eventually lead to a 'mutational meltdown' for populations with an effec tive size ..of <100" (Keller and Waller 2002 p230). Inbr eeding can be defined in a number of ways (Keller and Wall er 2002): � Pedigree inbreeding - Both parents share ancestors, and

the amount of inbreeding depends on the number of ancestors shared. An inbreeding coefficient (F) is calculated based on the probability of two genes at the same point on the chromosome being derived from the same gene in a common ancestor (known as "identical by descent"; IBD)(Keller and Waller 2002).

� Inbreeding as non-random mating - This is the degre e of

relatedness of mates relative to two mates chosen a t random in the population. An individual is inbred i f its parents are more closely related than two individuals chosen at random.

� Inbreeding because of population subdivision - Smal l

isolated populations can be inbred even with random mating because of the choices are restricted.

Inbreeding produces two genetic threats - the accumulation of damaging mutations, and the random loss of certain genes. This produces a reduction in evolutionary fitness known as "inbreeding depressio n" (Keller and Waller 2002). For example, a higher rat e of parasites and this reduced survival over winter in Soay sheep (Ovis aries) on a Scottish island (Coltman et al 1999). Crnokrak and Roff (1999) found statistically significant levels of inbreeding depression in 54% of species known to be inbred. Keller (1998) analysed the inbreeding coeffici ent of song sparrows on a Canadian island to quantify the


reduction in fitness. A mating between first degree relatives (eg: mother-son) reduced the hatching rat e by around one-half, and this became three-quarters wit h two generations of such matings. While among baboons where males mate with fema les in natal troops (close genetic relatives including siblings), infant mortality was 100% in two studies , but none at al in another (table 1.1).

(After Pusey and Wolf 1996)

Table 1.1 - Three studies of baboon inbreeding and infant mortality.

(Source: US Fish and Wildlife Service; public domai n)

Figure 1.1 - Olive baboon.

SPECIES FINDINGS STUDY

Olive baboon (Papio anubis)(figure 1.1)

4/4 inbred vs 6/32 outbred infants died in first month

Packer (1979)

Yellow baboon (Papio cynocephalus)

3/3 inbred vs 27/140 outbred infants died in first month

Alberta and Altmann (1995)

Chacma baboon (Papio cynocephalus ursinus)

No difference in mortality between inbred and outbred infants up to three months old

Bulger and Hamilton (1988)


Table 1.2 lists some of the criteria used and effects of inbreeding among birds, mammals, and poikilotherms (body temperature controlled by environment; eg: lizards) (Crnokrak and Roff 1999).

Table 1.2 - Criteria used to measure the effect of inbreeding in different species. Table 1.3 gives examples of studies showing ef fects of inbreeding in different animals.

(After Keller and Walter 2002)

Table 1.3 - Examples of studies on effect of inbree ding in a population. Table 1.4 gives some examples of studies showi ng specific inbreeding relationships in different anim als.

ANIMAL RISK STUDY

Blue tit (Cyanistes caeruleus)

Reduced hatching rate Kempenaers et al (1996)

Common shrew (Sorex araneus)

Survival to maturity; body length

Stockley et al (1993)

Harbour seal (Phoca vitulina)

Birth weight; neonatal survival

Coltman et al (1998)

Black-footed rock wallaby (Petrogale lateralis)

Fecundity (ie: amount of offspring)

Eldridge et al (1999)

BIRDS MAMMALS POIKILOTHERMS

� Clutch/brood size � Nestling survival � Number of eggs

hatched � Number of young

fledged � Hatching success

� Juvenile survivorship

� Probability of producing litter

� Litter size � Juvenile weight � Number of emergent

young � Percentage of

emergent young � Ejaculation volume � Sperm motility � Sperm

abnormalities � Body mass

� Number of clutches � Clutch size � Hatching success � Number of dead

embryos � Percentage fry

survival � Growth of adults


(After Pusey and Wolf 1996)

Table 1.4 - Nature of inbreeding relationship and consequences in three studies. Though inbreeding has risks with "severely deleterious recessive alleles" 1 (Pusey and Wolf 1996)(figure 1.2), it can have advantages (table 1. 5).

(Source: Imaginary Friend; public domain)

Figure 1.2 - Inbreeding and recessive gene example.

1 Allele is a possible copy of a gene at a particular point of the chromosome.

ANIMAL RELATIONSHIP FINDINGS STUDY

Golden lion tamarin (Leonpithecus rosalia)

Father-daughter; siblings

14/14 inbred vs 1/5 outbred infants died before weaning

Dietz and Baker (1993)

Cooper's hawk (Accipiter cooperii)

Grandmother-grandson

Low hatching rate Rosenfield and Bielefeldt (1992)

White-footed mice (Peromyscus leucopus noveboracensis)

Siblings Lower survival rate when individuals born in captivity released into wild

Jiménez et al (1994)


ADVANTAGES 1. In small, isolated populations genetic relatives may be the only potential mates available. So it is better to mate with the risk for the offspring than to not mate at all. 2. Evolutionary advantages to inbreeding. In eusoci al species, like ants, inbreeding is very high because only one fema le and a limited number of males mate. Among naked mole-rats (Hetero cephalus glaber)(figure 1.3), that live in subterranean colo nies in north-east Africa, "DNA fingerprinting" showed a mean relatedn ess of 0.81 (81%) (Reeve et al 1990). Altruistic behaviour becomes an advantage for individuals. Young from previous litters maintain the colony and raise the newborns. There is an evolutionary advantage to car ing for siblings, who are genetically as similar, compared to having own offspring (50% similar to parents). 3. Choices limited for animals to seek non-relative mates including predator pressure, scarcity of food, and physical b arriers to movement (Reeve et al 1990). 4. Risks of outbreeding including genetic incompati bility, pathogens, and mismatch between parents which limit parenting success (Pusey and Wolf 1996). Cohen and Dearborn (2004) reported that frigatebirds (Fregata minor) appeared to actively choose genetic ally similar mates (Box 1.1). DISADVANTAGES 1. Inbreeding depression; ie: reduced evolutionary fitness including sperm deformities, sterility, and decline in courts hip frequency (Pusey and Wolf 1996). 2. Greater chance of young not surviving to adultho od; eg: inbred red-cockaded woodpeckers (Picoides borealis) in sou th-eastern USA have reduced hatching rates and fledgling survival (Daniels and Walters 2000). 3. Increased extinction risk, particularly for smal l populations, through reduced survival of young and shorter lifes pan of survivors. 4. Reduced survivorship generally. A study of forty captive inbred populations showed an average increase in mortality of 33% compared to outbred populations (Ralls et al 1988). Jiménez et al (1994) followed the survival of captive-born White-footed mice (Peromyscus leucopus novaboracens is) over ten weeks after introduction to the wild at fields near Chica go Zoological Park, Brookfield, Illinois, USA. On average, surviv al of inbred mice was 56% that of non-inbred ones, mainly due to a gr eater loss of body mass by the former group. 5. Greater susceptibility to changes in the environ ment; eg: more inbred song sparrows (Melospiza melodia) died durin g storms on Mandarte Island, Canada (Keller et al 1994). Table 1.5 - Advantages and disadvantages of inbreed ing.


(Source: Ltshears - Trisha M Shears; public domain)

Figure 1.3 - A naked mole-rat.

Box 1.1 - Details of Cohen and Dearborn (2004).

Great frigatebirds (figure 1.4) breed on remote isl ands in the Pacific and Indian Oceans, and show natal site fidelity (ie: breed close to where born) which is a risk factor for inbreeding. But on Tern Island (one of t welve small islands in the French Frigate Shoals atoll, northwestern Hawaiian islands, USA), where the popu lation is studied, there is enough movement of males to counteract this risk (Cohen and Dearborn 2004). So if inbreeding occurs, it must be by female choice. Cohen and Dearborn (2004) collected blood samples f or DNA fingerprinting from 92 family groups in 1998 and 19 99. Genetic similarity between mates was greater than e xpected by chance (mean relatedness of 0.082; significantly different to zero) suggesting inbreeding. The autho rs concluded: "Although the potential for fitness consequences of this inbreeding remains unclear, th e occurrence of inbreeding in this population is intr iguing because it is likely to be the result of a active m ate choice process" (p1234).


(Source: Jason Corriveau; in public domain)

Figure 1.4 - Male great frigatebird displaying. The benefits of inbreeding can be assessed in relation to two situations (Kokko and Ots 2006): a) Simultaneous choice scenario - Choice betwe en incestuous and non-incestuous mating; b) Sequential choice scenario - Choice between mating with kin now or waiting for non-kin to appea r. In the second situation, waiting for non-kin i s risky because they may not appear or the individual may die before their arrival. So inbreeding makes sense in the sequential choice scenario. With the simultaneous choice scenario, inbreed ing can make sense for the parent who cares for the offspring. A female who has a period of pregnancy a nd after-birth care is not able to mate again for a wh ile. This is a "time out" (Kokko and Ots 2006). If such a female has mated with a related male, who then mate s with unrelated females, she has gained indirect fitness from inbreeding. Indirect fitness refers to benefits at the level of the gene.


1.2. AVOIDING INBREEDING 1. One way of avoiding inbreeding is through natal dispersion. At a certain time, juveniles are sent o r choose to leave their group or site of birth. For example, male and female juvenile meadow v oles (Microtus pennsylvanicus) were found to be more lik ely to disperse when released into a empty area with sibli ngs than with non-siblings (Bollinger et al 1993). But dispersal has costs including predation ri sk, energy expenditure, inability to survive in new environments, and incompatibility with non-related mates. Thus some species choose mates of "intermediate relatedness" (Pusey and Wolf 1996). For example, fe male white-footed mice preferred to mate with unfamiliar first cousins than unfamiliar siblings or unfamiliar unre lated males (Keane 1990), and similarly Japanese quail fe males (Bateson 1982). Ekernas and Cords (2007) studied natal dispers ion at between 6-8 years-old by young male blue monkeys (Cercopithecus mitis stuhlmanni) in the Kakamaga Fo rest, Kenya. Twenty-six natal dispersions were observed a mong three studied groups (each group ranging from thirt y-three to sixty-five individuals). Four factors were analysed to explain the disp ersal process: i) Dispersed males hounded out by adult males - This did not seem to be important as there was no differ ence in aggressive encounters between adult males and individuals who subsequently did or did not leave t he group. ii) Dispersed males did not have mating opportunities - If this was the case, dispersion wo uld occur during the mating season, and it did not more often than expected by chance. iii) Dispersed males have weaker social ties t o the group - Dispersing and non-dispersing males did not vary in their social behaviour, but time spent in social activities (eg: grooming) was significantly greater for juvenile females compared to juvenile males. iv) Environmental factors involved - Male disp ersal was more often during the dry season, and least lik ely when food was scarce. This would suggest that dispe rsion took place when the movers had a better chance of b eing accepted by the new group (ie: not during food shortages).


January was the month with the highest number of dispersals observed (n = 7), when rainfall was low and fruit availability generally high (table 1.6).

Table 1.6 - Distribution of dispersals in three sea sons. The authors felt that hormonal or biochemical changes associated with puberty played a role in triggering the process. In terms of inbreeding, the triggering process evolved to reduce the risk. Male spotted hyenas (Crocuta crocuta) leave th e female socially dominated "clans". Höner et al (200 7) analysed ten years of data on the hyena population of Ngorongoro Crater, Tanzania (370 individuals in eig ht clans), and found 90% of males dispersed. Females mate with several males which means th at female offspring may not be able to recognise their genetic father, so they follow the rule: "avoid mal es that were members of your group when you were born and favour males that were born into or immigrated into your group after your birth" (p798). Data showed that 90 % of litters were from males born into or immigrated int o the female's group after her birth. Only two litters (o f 309) were cubs from daughter-father matings. 2. Another way to overcome the risk of inbreeding i s female extra-pair copulations with males from outsi de the natal group. For example, splendid fairy wrens (Malurus splendens) were estimated to have breeding pairs wi th close relatives in 25% of cases (compared to the av erage of 5% in other paired species; Pusey and Wolf 1996) , but "DNA fingerprinting" showed evidence of eggs in the nest not sired by the resident male (Rowley et al 1993). 3. Kin recognition, through smell, for example, is important.

PERIOD CHARACTERISTIC NUMBER OF DISPERSALS

SIGNIFICANCE COMPARED TO CHANCE

May-Sept Most conceptions

7 ns

Dec-Feb Lowest average rainfall

16 more; p<0.0001

June-August Food shortages 1 ns


Experiments place related individuals together or unrelated individuals to measure reproductive rates , which are lower among the related group, or individ uals are offered a choice of mates of varying genetic relatedness. For example, wild house mice (Mus musc ulus) in sibling groups were less likely to produce litte rs compared to cousin groups or non-relatives (Krackow and Matsuschak 1991). While female mice given a choice of familiar siblings, non-familiar siblings, and non-siblings preferred the latter for mating (Dewsbury 1988).

4. Delayed sexual maturation in the presence of clo se relatives; eg: marmosets and tamarins in the presen ce of opposite sex parents and siblings in their group. 1.3. ADAPTATIONS WITH INBREEDING In animals that show inbreeding, their behavio ur may be different with kin - for example, ejaculating le ss sperm. Lewis and Wedell (2009) found that Indian me al moth (Plodia interpunctella)(figure 1.5) males ejac ulated 54% less sperm when mating with sisters compared to unrelated females. These male moths transfer sperm to the female in a spermatophore, which contains the distinctively dif ferent fertile and non-fertile sperm. Sisters received significantly less fertile and non-fertile sperm (t able 1.7).

Table 1.7 - Approximate mean number of sperm provid ed to unrelated and related females. Sperm production is costly for male moths who can mate only a handful of times (maximum eight; Ryne e t al 2001) in their short lives (12 days average). Males also vary their ejaculation depending on the quality/fec undity of the female, and the presence of other males (spe rm competition)(Lewis and Wedell 2009). But in red junglefowl (Gallus gallus), Pizzari et al (2004) found that males inseminated sisters with mo re sperm that unrelated females. This was because fema les have the ability to store sperm from multiple males and can "choose" which male's fertilises the eggs. This is a strategy for females to deal with the risk of inbre eding (Tregenza and Wedell 2002).

TYPE OF SPERM RELATED FEMALES UNRELATED FEMALES

Fertile 3000 4000

Non-fertile 30 000 45 000


(Source: Kaldari; in public domain)

Figure 1.5 - Indian meal moth. 1.4. AMUR LEOPARDS The Amur (or Far Eastern) leopard (Panthera pa rdus orientalis) may be reduced to less forty wild indiv iduals alive in the Russian Far East (Uphyrkina et al 2002 ). When a population is small the opportunities f or breeding are limited, and this can lead to mating w ith close genetic relatives Inbreeding). Inbreeding inc reases the risk of recessive genes (those needing both cop ies of the gene to manifest the effect) and congenital pro blems


(eg: bone deformity). Also a decrease in litter siz e has been reported by field researchers (from two in 197 3 to one in 1997)(Uphyrkina and O'Brien 2003). Uphyrkina and O'Brien (2003) found that wild A mur leopards from the Primorskiy Kray area of Russia an d North Korea showed lower genetic variation than cap tive populations from zoos worldwide, and relatedness va lues of between 60-90% 2. The documentary, "The Last Leopard" (Director: Tatsuhiko Kobayashi), filmed Amur leopards in Kedro vaya Pad Natural Reserve, west of Vladivostok, Russia. T he documentary reported genetic analysis of seven anim als which showed inbreeding (figure 1.6).

Figure 1.6 - Genetic relationship between seven Amu r leopards in Kedrovaya Pad Natural Reserve.

2 100% = identical twins; 50% = parent-offspring and between siblings.


In figure 1.6, four matings are key: (i) Outbreeding. Two genetically unrelated individuals (Ugraty and Starshuka) mate and their offspring (Sbetlana and Puzan) will each share 50% of the genes of each biological parent. (ii) Inbreeding. The father (Ugraty) mates wit h his daughter (Sbetlana) producing female offspring (Marshuka). This gives a coefficient of inbreeding of 25%. This is the chance of getting two copies of a gene that are from the same ancestor. (iii) Inbreeding. Marshuka mates with her half -sibling (Puzan) to produce female offspring (Skrytn aya). Half-siblings normally share 25% of the same gene ( and full siblings 50%). The coefficient of inbreeding i s 12.5% here. (iv) Inbreeding. The father (Puzan) mates with his daughter (Skrytnaya) to produce cub 3. 1.5. REFERENCES Abbott, D.H (1993) Social conflict and repro ductive suppression in marmoset and tamarin monkeys. In Mason, W.A & Mendo za, S.P (eds) Primate Social Conflict New York: State University of New York Press Alberta, S.C & Altmann, J (1995) Balancing c osts and opportunities: Dispersal in male baboons American Naturalist 145, 279-306 Bateson, P (1982) Preferences for cousins in Japanese quails Nature 295, 236-237 Bollinger, E.K et al (1993) Inbreeding avoid ance increases dispersal movements of the meadow vole Ecology 74, 1153-1156 Bulger, J & Hamilton, W.I (1988) Inbreeding and reproductive success in a natural chacma baboon Papio cynocephalus ursin us population Animal Behaviour 36, 574-578 Cohen, L.B & Dearborn, D.C (2004) Great frig atebirds, Fregate minor, choose mates that are genetically similar Animal Be haviour 68, 1229-1236 Coltman, D.W et al (1998) Birth weight and n eonatal survival of harbour seal pups are positively correlated with ge netic variation measured by microsatellites Proceedings of the Royal Society of London B, Biological Sciences 265, 803-809 Coltman, D.W et al (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population Evol ution 53, 1259-1267 Crnokrak, P & Roff, D.A (1999) Inbreeding de pression in the wild Hereditary 83, 260-270 Daniels, S.J & Walters, J.R (2000) Inbreedin g depression and its

3 Details of conservation efforts at http://www.amur.org.uk/leopards.shtml and http://www.amur-leopard.org/.


effects on natal dispersion in red-cockaded woodpec kers Condor 102, 482-491 Dewsbury, D.A (1988) Kin discrimination and reproductive behaviour in muroid rodents Behavioural Genetics 18, 525-536 Dietz, J.M & Baker, A.J (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus ros alia Animal Behaviour 46, 1067-1078 Ekernas, L.S & Cords, M (2007) Social and en vironmental factors influencing natal dispersal in blue monkeys, Cercop ithecus mitis stuhlmanni Animal Behaviour 73, 1009-1020 Eldridge, M.D.B et al (1999) Unprecedented l ow levels of genetic variation and inbreeding depression in an island po pulation of the black-footed rock wallaby Conservation Biology 13, 531-541 Höner, O.P et al (2007) Female mate-choice d rives the evolution of male-biased dispersal in a social mammal Nature 448, 798-801 Jiménez, J.A et al (1994) An experimental st udy of inbreeding depression in a natural habitat Science 266, 271-273 Keane, B (1990) The effect of relatedness on reproductive success and mate choice in the white-footed mouse, Peromyscus l eucopus Animal Behaviour 39, 264-273 Keller, L.F (1998) Inbreeding and its fitnes s effects in an insular population of song sparrows (Melospiza melodia) Evo lution 52, 240-250 Keller, L.F & Waller, D.M (2002) Inbreeding effects in wild populations Trends in Ecology and Evolution 17, 5, 230-241 Keller, L.F et al (1994) Selection against i nbred song sparrows during a natural population bottleneck Nature 372, 356-357 Kempenaers, B et al (1996) Genetic similarit y, inbreeding and hatching failure in blue tits: Are unhatched eggs infertile? Proceedings of the Royal Society of London B, Biological Sciences 263, 179-185 Kokko, H & Ots, I (2006) When not to avoid i nbreeding Evolution 60, 3, 467-475 Krackow, S & Matuschak, B (1991) Mate choice for non-siblings in wild house mice: Evidence from a choice test and a repro duction test Ethology 88, 99-108 Lewis, Z & Wedell, N (2009) Male moths reduc e sperm investment in relatives Animal Behaviour 77, 6, 1547-1550 Packer, C (1979) Inter-troop transfer and in breeding avoidance in Papio anubis Animal Behaviour 27, 1-36 Pizzari, T et al (2004) Sex specific, counte racting responses to inbreeding in a bird Proceedings of Royal Society o f London, Series B 271, 2115-2121 Pusey, A & Wolf, M (1996) Inbreeding avoidan ce in animals Trends in Ecology and Evolution 11, 5, 201-206 Ralls, K et al (1988) Estimates of lethal eq uivalents and the cost of inbreeding in mammals Conservation Biology 2, 185-193 Reeve, H.K et al (1990) DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-r at Proceedings of the National Academy of Sciences, USA 87, 2496-2500 Rosenfield, R.N & Bielefeldt, I (1992) Natal dispersion and inbreeding in the Cooper's hawk Wilson Bulletin 104, 182-184 Rowley, I et al (1993) Inbreeding in birds. In Thornhill, N.W (ed) The


Natural History of Inbreeding and Outbreeding: Theo retical and Empirical Perspectives Chicago: University of Chicago Press Ryne, C et al (2001) Spermatophore size and multipl mating: Effects on reproductive success and post-mating behaviour in t he Indian male moth Behaviour 138, 947-963 Stockley, P et al (1993) Female multiple mat ing behaviour in the common shrew as a strategy to reduce inbreeding Pro ceedings of the Royal Society of London B, Biological Sciences 254, 173-179 Tregenza, T & Wedell, N (2002) Polyandrous f emales avoid costs of inbreeding Nature 415, 71-73 Uphyrkina, O & O'Brien, S.J (2003) Applying molecular genetic tools to the conservation and action plan for the critically endangered far Eastern leopard (Panthera pardus orientalis) Comptes rendus -Biologies 326, S93-S97 Uphyrkina, O et al (2002) Conservation genet ics of the Far Eastern leopard (Panthera pardus orientalis) Journal of Her editary 93, 5, 303-311 (Freely available at http://jhered.oxfordjournals.org/cgi/reprint/93/5/3 03)


2. ADVANTAGES AND DISADVANTAGES OF MONOGAMY 2.1. Introduction 2.2. Monogamy 2.3. Monogamy and the vole 2.4. Extra-pair copulations 2.4.1. Evaluation of Hill et al (1994) 2.5. Extra-pair copulations and apes 2.6. References 2.1. INTRODUCTION Monogamy involves mating (and often parental c are) by one male and one female for a breeding season or for life. It is the form of social organisation found i n about 3% of mammals (Young et al 1998), but in 15% of primates (Reichard 1995). The alternatives are polygamy (mating with mul tiple individuals who help in caring for the young), or promiscuity, which is multiple-partner matings with out any post-copulation relationship. The best strategy will also vary between males and females (table 2.1). MALE 1. Monogamy: one partner for breeding season a. Mate-assistance monogamy Male as sists female in chil d-rearing b. Mate-guarding monogamy Female dispersal 2. Polygyny: one male with multiple females a. Female defence polygyny Male de fends cluster of fema les b. Resource defence polygyny Male de fends resourc es and females come c. Lek polygyny Male de fends territo ry and females come to mate only d. Scramble competition polygyny Males f ind scattered females FEMALE 1. Monogamy a. Female-enforced monogamy Male ke eps other females away and assists in child- rearing


2. Polyandry: one female with multiple males a. Fertility-insurance polyandry Greater fertilisation of eggs b. Better sperm polyandry Genetic ally diverse sperm c. More material benefits polyandry More re sources from males d. More paternal care polyandry More ma les help in child-r earing (After Alcock 1993)

Table 2.1 - Types of mating strategy. The best strategy for passing the genes into t he next generation will vary between the male and fema le of the species. The male is able to produce many sperm , and so can theoretically have as many offspring as mate s found. But the female is restricted, in most species, by giving birth to the offspring. Thus she has more in vested in its survival (table 2.2). Different species behave in different ways dep ending upon their environments, but generally the example in table 2.2 is the common strategy of sexual selectio n. "Female choosiness" has led to the evolution of mal es who compete, in some way, to show the female that their genes are best for mating. This competition involves figh ts, "shows of quality" (eg: ornaments like a peacock's tail), or the collection of scare resources to give to the female ("resource-holding power"; RHP). EXAMPLE - Male mates with ten females, who ha ve one offspring each in the breeding seas on OFFSPRING STRATEGY MALE 10 fathered; can Find many female mates; ie: afford some not indiscriminate; l ittle concern to survive for post-natal ca re FEMALE Each female has Female invests ti me and effort one offspring in survival, but must exercise and thus survival choosiness about male; ie: only important mate with male wh o has "best genes" Table 2.2 - Sexual selection and strategies for mal es and females. Table 2.3 shows the factors that influence mat ing


strategies. WHY WHY WHY WHY WHY WHY MALE FEMALE ONE ONE MALE FEMALE STAYS STAYS MALE FEMALE EXCLUSI VE EXCLUSIVE 1. X 2. X 3. X 4. X 5. X X X X X X 6. X X X 7. X X X 1 = Matneral care needed 2 = Paternal care needed 3 = Geographical distribution of breeding females e g sparse 4 = Geographical distribution of breeding males 5 = Resource distribution eg limited 6 = Male-male aggression 7 = Female-female aggression (After Gowaty 1996) Table 2.3 - Factors influencing mating strategies. 2.2. MONOGAMY There are different types and explanations of monogamy including obligate and facultative (Kleitm an 1977). The former relates to the need of the offspr ing to be cared for by both parents. Facultative monogamy is where males cannot monopolise more than one female because the females are geographically dispersed (K omers and Brotherton 1997). Komers and Brotherton (1997) compared these tw o types of monogamy in different mammal species. "Pat ernal care was considered to be present if males of that species are known to retrieve young, transport youn g, or provide food" (p1261). Monogamy was found to exist significantly more often in the absence of parental care than in the presenc e of it. "For a general theory on the evolution of monog amy in mammals, we must therefore focus on factors other t han paternal care that may have promoted monogamy" (Kom ers and Brotherton 1997 p1267). Monogamy was also not c ommon in species with geographically dispersed females, b ut it was more common where females were solitary living in small, exclusive territories that males could monop olise. Staying with one female reduced the risk and costs for


males of searching for multiple females. Table 2.4 summarises the main advantages and disadvantages of monogamy. ADVANTAGES 1. Know quality of partner and their genes. 2. Usually help with rearing young, which is crucia l when biparental care is required. 3. Less risk of female-female and male-male aggress ion compared to polygamy. 4. A strategy that can be short-term (one breeding season) or long-term (for life). 5. Less risk of infanticide than with polygamy. 6. Best strategy for males if females are geographi cally dispersed and/or scarce. 7. Males can be certainty of their paternity compar ed to polyandry. DISADVANTAGES 1. Fear of extra-pair copulations, and males, in pa rticular, end up caring for non-genetic offspring. 2. Lack of variety of genes over multiple breeding seasons. 3. If male partner infertile, for example, female w ill be unfertilised. 4. Cost of mate-guarding for males. 5. If no mate than no breeding that season. 6. Often involves courtship and displays which have costs. 7. Limits to amount of offspring per breeding seaso n, particularly for males, compared to polygamy. Table 2.4 - Advantages and disadvantages of monogam y. Where animals are monogamous, there is usually a complex system of courtship - a series of tests for males to show to the females their commitment to her and the care of the young as well as the quality of their g enes (table 2.5). 1. Ensures pairing with the right species 2. Permits survival in aggressive species; ie: to approach without being att acked 3. Display of fitness 4. Improves species; ie: only fittest survive Table 2.5 - Functions of courtship.


Potential mates have to "establish clues to sp ecies identification, genetic superiority, and complement arity to the selecting individual, and for species with parental care, the quality and quantity of care an individual is likely to provide" (Burley 1981 p515) . So in many species, it is possible that multiple crite ria are used for mate selection. Burley (1981) compared mate choice by pigeons using three sets of criteria: i) Plumage colour ("blue" or "ash-red") and pa ttern ("checker" or "bar"); ii) Age and reproductive experience - "Super-experienced (eight or more clutches), "semi-experie nced (1-2 clutches), or "no experience. (Experience lead s to more efficient breeding (eg: fledge heavier young), but a reduced breeding rate; iii) Relative dominance position - Preference for dominant individuals or individuals of the same ran k. The preference for these different characteris tics was tested by giving a pigeon ("chooser") a choice of two opposite-sex birds with differences in specific way s. Table 2.6 summarises the findings in the choice tes ts.

Table 2.6 - Preferences by pigeons on choices of individual characteristics. All the individual preferences were combined i nto a selectivity index, which showed that females were m ore selective than males. This fits with the prediction that the sex who makes the greater parental investment w ill be more selective (Trivers 1972); ie: females in monog amy. However, Burley (1981) admitted that selectivi ty is

MALE PREFERENCES FEMALE PREFERENCES

Plumage Blue over ash-red Blue checker over blue bar; blue bar over ash-red bar or checker

Age and experience

More experienced; experience more important than age; Less experienced young over super-experienced old

More experienced; experience more important than age; Less experienced young over super-experienced old

Dominance No preferences Experienced females preferred dominant males; inexperienced females no preference


not necessarily constant over time, and may vary wi th length of time since heterosexual contact, and seas on. For example, with the latter, males had stronger preferences in August-October than in January-March . 2.3. MONOGAMY AND THE VOLE The vole of North America is interesting to st udy in relation to social organisation because different s pecies show completely different behaviours. The prairie v ole (Microtus ochrogaster)(figure 2.1) is monogamous, w hile the montane vole (Microtus montanus) is promiscuous (table 2.7).

Table 2.7 - Differences in social organisation betw een two species of voles.

(Source: US National Park Service; in public domain )

Figure 2.1 - Prairie vole. The difference between the two species of vole s has been explained by the hormones, oxytocin and vasopr essin. Oxytocin triggers maternal behaviour, and partner preference in female prairie voles. While vasopress in triggers paternal care, and partner preference in m ale prairie voles (Young et al 1998). Research has shown that in prairie voles copul ation

PRAIRIE VOLE MONTANE VOLE

Mating system

Monogamy Promiscuous

Parental care

Both parents involved in prolonged care of offspring

Mother only, but even she abandons young soon after birth

Behaviour High level of social contact as species (50% of time in contact in experiments). Paired males aggressive towards other members of species

Low level of social contact (5% of time). Live in isolated burrows.


triggers oxytocin release because where it is block ed by drugs, the female does not stay with the male after mating (Williams et al 1994). The prairie vole brai n has oxytocin receptors in areas in the brain related to reward (mesolimbic dopamine reward pathway) which conditions the female to the odour of her mate. The montane vole has less such receptors (Young et al 1 998). Injections of oxytocin in unmated females and vasopressin in unmated males produces a preference for cagemates (Young et al 1998). But injections of vasopressin into male montane voles produced increa sed autogrooming only (Young et al 1997). 2.4. EXTRA-PAIR COPULATIONS Sexual selection explains the different strate gies by males and females of a species when looking for a mating partner. For example, female choosiness lead s to the evolution of males who can display their good q uality genes in obvious ways, like the strength of calls o r visual "ornaments", or males who provide resources to support the female during pregnancy and after birth . In a polygynous system, where females mate wit h multiple males, sexual competition among males will be high. But in monogamous species, partner choice may be limited and so it is better to have any mate than n ot breed. However, female extra-pair copulation (EPC) widens the choice of genes, particularly if the male breed ing partner has low quality genes (Hill et al 1994). So males need still to signal their quality of genes. For ex ample, male barn swallows with longer tail streamers (sign al of good genes) engage in more EPCs than short-tailed m ales (Moller 1988). Where male care is essential, this will influ ence females from seeking EPCs (figure 2.2). MALE CARE ESSENTIAL MALE CARE NOT ESS ENTIAL ↓ ↓ FEMALE EPC COST NO OR LOW EPC COS T = LOSS OF MALE CARE ↓ ↓ FEMALE DON'T SEEK EPC FEMALE SEEKS EPC ↓ ↓ EXTRA-PAIR PATERNITY EPP OCCURS (EPP) RARE ↑ ↑ NO SELECTION PRESSURE STRONG SELECTION PRESSURE ON MALES AS EPC PARTNER ON MALES AS EPC P ARTNER (After Birkhead and Moller 1996) Figure 2.2 - Females seeking extra-pair copulations .


Hill et al (1994) investigated female EPC amon g house finches (Carpodacus mexicanus)(figure 2.3) in one breeding season (1991) at the University of Michiga n, Ann Arbor, USA. The bright plumage of the males is an " honest signal" of gene quality and parental investment. Ma les with brighter plumage have been observed to feed incubating females more than males with dimmer plum age (Hill 1991).

(Source: Public domain)

Figure 2.3 - Male house finch. Hill et al scored the plumage brightness 4 of both sexes on seven areas of the body (four on the under side, crown, eyestripe, and rump) to give a single index of overall plumage brightness. Blood samples were also taken for "DNA fingerprinting" to establish paternity. Br oods from thirty-five nests were analysed (n = 119 chick s). It was expected that males with dull plumage will be cuckolded more. Ten chicks (8.4%) in five different nests were clearly fathered by a male other than the attending male at the nest. There was no difference in plumage brightness scores, wing length, and age of cuckolde d and non-cuckolded males. The results were not as expect ed, and the only variable showing a significant differe nce

4 The plumage colour varies from pale yellow to bright red (Hill 1992).


was nest dispersion - all illegitimate nestlings we re in closely dispersed nests. If there is no difference in plumage brightnes s and cuckoldry, the authors asked, why would bright plum age evolve in male house finches. One answer is that th ere are more males than females (sex ratio of 1.52 male s to one female), and so males are competing to find a m ate. Also brighter plumage males mate earlier in the bre eding season (by as much as 100 days at the extremes), an d this would allow more broods per season. 2.4.1. Evaluation of Hill et al (1994) 1. Most of the birds were captured in traps or mist nets (figure 2.4) in order to fit with coloured leg band s for identification purposes. Though this is a common practice, what is the effect upon the birds?

(Source: Julio Reis)

Figure 2.4 - Bird trapped in mist net. 2. The overall plumage brightness index score was b ased on adding 21 individual scores together - seven reg ions of the body and scores for hue, intensity, and tone 5 for each as compared to colour slides in the "Methuen Handbook of Colour" (Kornerup and Wanscher 1983). T he reliability of such a score could be open to questi on. 3. The effect on the birds of taking a blood sample . The chicks were sampled 8-10 days after hatching. 4. The authors admitted: "Date of capture is potent ially important in a study of paternity. If a female or h er mate is detained during the female's fertile period , observer-induced EPCs may result. Most birds in thi s study were sampled before the start of nest-buildin g or after egg-laying was complete when handling should not have affected paternity. However, a few males and f emales were just captured just prior to or during egg-layi ng, so we also looked for an effect of capture date on

5 Hue scores ranged from colourless (1) through yellow (2-4), orange (5-8), to red (9-11). Intensity was scored from 1 to 8, and tone from 1 to 6 (Hill 1992).


cuckoldry" (Hill et al 1994 p194). 5. Standard procedures of the time were used for "D NA fingerprinting" and thus calculating paternity. How ever, the cost of the process was high and this limited t he sample size of the study. 6. One-tailed tests were used for statistical analy sis as a clear prediction of duller plumage males experien cing more cuckolds was made (one-tailed research hypothe sis). One-tailed tests have less risk of a Type I error (claiming a significant result when the findings we re due to chance; ie: non-significant). 7. The differences between cuckolded and non-cuckol ded males were statistically analysed with the Mann-Whi tney U test (table 2.8). This test was used because the pl umage brightness index score can be classed as ordinal da ta, and thus a parametric statistical test could not be used. The Mann-Whitney test is ideal for comparing groups of different sizes (table 2.9).

(* = U value must be less than critical value to be significant. Critical values taken from Coolican 1990).

Table 2.8 - Non-significant results from Mann Whitn ey tests comparing cuckolded and non-cuckolded males.

Table 2.9 - Main advantages and disadvantages of th e Mann Whitney U test.

COMPARISON "U" VALUE

PROBABILITY SIZE OF GROUPS (N)

CRITICAL VALUE*

Plumage brightness score

62 0.44 5, 26 27

Wing length 40.5 0.11 5, 25 27

Female plumage colouration

29.5 0.30 5, 17 17

Clutch initiation date

55 0.59 5, 26 27

Clutch size 41.5 0.30 5, 23 24

Male age 56 0.31 5, 26 27

ADVANTAGES DISADVANTAGES

1. Does not need groups to be of equal size. 2. Good with small samples. 3. Not restricted by parametric criteria.

1. Not as efficient as parametric tests. 2. Deals with relative positions not absolute scores. 3. Problems if too many tied


8. The sample size of cuckolded males was low (n = 5) which could mean that there is low statistical powe r in the statistical analysis. This means that the stati stical test is limited in its ability to find a significan t difference in the data. 9. The means of the plumage brightness scores were used, whereas the median may have been better (table 2.10 ).

Table 2.10 - Mean and median as measures of central tendency. 10. The differences were presented graphically with box-plots, which show the distribution of the scores wi th 10th, 25th, 50th, 75th and 90th percentiles. Howeve r, this can be distorted by the small number of cuckol ded males (table 2.11). MALE PLUMAGE BRIGHTNESS SCORE MAL E AGE (YEARS) NON-CUCKOLDED* CUCKOLDED* NON CUCKOLDED 10th 120 133 1.0 1.0 25th 135 141 1.0 1.0 50th 145 144 2.0 2.0 75th 153 150 3.0 4.1 90th 157 150 4.0 4.6 (* n = 26; ** n = 5) (After Hill et al 1994)

Table 2.11 - Distribution of scores from box-plots of cuckolded and non-cuckolded males.

MEAN MEDIAN

Definition Add up scores and divide by number of scores.

Put data into order and take middle number.

Advantages 1. Most sensitive measure of central tendency. 2. Total and all values taken into account.

1. Shows exact middle point with 50% above/below. 2. Unaffected by extreme values in one direction.

Disadvantages 1. Not good if extreme scores or scores vary greatly as with small samples. 2. Not good with highly skewed distributions.

1. Less information used than the mean. 2. Time consuming to rank large sets of data.


2.5. EXTRA-PAIR COPULATIONS AND APES Reichard (1995) reported EPCs among three fami lies of white-handed gibbons (Hylobates lar)(figure 2.5) observed in Khao Yai National Park,Thailand (table 2.12).

Table 2.12- Details of three family groups observed by Reichard (1995).

(Source: Ltshears)

Figure 2.5 - White-handed gibbon.

GROUP SIZE ADULT MALE ADULT FEMALE

A 4 Fearless Andromeda

B 5 Bard Bridget

C 6 Cassius Cassandra


Among these long-term monogamous primates, obs erved daily for nearly eighteen months between January 19 92 to August 1993, three EPCs were witnessed: Andromeda a nd Cassius twice, and Andromeda and Bard. Reichard's f ield notes described the last occasion thus: " [0645h] Immediately, a copulation in a dorso-ventral positi on followed. It lasted only a few seconds, because [Fearless] - who probably detected the EPC - charge d towards the couple and vigorously pursued the escap ing [Bard] for more than 30 minutes" (p106). The EPCs were only 12% of all copulations obse rved by Reichard (1995), the majority were with the pair ed male (76 of 82). Though the female may gain other g enes from an EPC, there is a risk of injury in the activ ity and her partner may then seek EPCs (table 2.13). Th e evolutionary response to female EPCs for males is m ate-guarding and retention behaviour.

Table 2.13 - Advantages and disadvantages of EPCs f or females in monogamous species. The Reichard (1995) study is an example of a naturalistic observation over a long period by the researcher, which collects qualitative data (that c an be converted into quantitative data later). This type of study has advantages and disadvantages (table 2.14) .


1. To gain better genes. 2. To gain a variety of genes, particularly if inbreeding involved. 3. To increase sperm competition and consequently reproductive rate. 4. To lower the risk of infanticide if EPC male becomes mate. 5. The fear of EPC can encourage the mate to copulate more, and mate-guarding behaviour.

1. Risk that male partner will engage in EPC. 2. Risk that partner may leave offspring (mate desertion). 3. Risk of injury during EPC. 4. Risk of injury from mate. 5. Risk of diseases and pathogens.


Table 2.14 - Advantages and disadvantages of Reicha rd's (1995) naturalistic observation method. In a similar study of white-handed gibbons and siamang (Hylobates syndactylus)(figure 2.6) over 2. 5 years at the Ketambe Research Station, Sumatra, Indonesia, Palombit (1994) observed five episodes o f EPC. These involved a female siamang mating with three m ales from a neighbouring group at different times (table 2.15).

Table 2.15- Five EPCs by female siamang from C grou p. The "C" female "played a role in initiating th em by: (1) maintaining proximity to the territorial border where a male from a neighbouring group could gain sexual access to her (which sometimes involved moving towards the male); (2) not avoiding an extra-group male that approached her; and (3) directing the.. 'solicitati on' gesture at some extra-group males.." (p722). This f emale may have been motivated to find EPCs because she pr oduced a premature stillborn and no other offspring during the study.


1. Very detailed study of gibbons over long periods of time. 2. All observations are recorded for later analysis. 3. The observer is able to recognise individual animals and record their behaviour.

1. Depends upon the observer; ie: information may be missed because of the focus on one event or that it takes place outside the observer's field of view. 2. The animals were well habituated to human observers, but does the presence of such observers change the gibbons' behaviour? 3. Very time consuming for the researcher.

EPC WITH: DATE

Immature male of P group (3 times)

15 February 1986 7 August 1986 26 September 1986

Adult male: mate of P group 9 April 1986

New adult male: mate of P group 9 February 1987


(Source: Vassil; in public domain)

Figure 2.6 - Siamang. In both this study and Reichard (1995), the EP Cs were rare, but it does not mean "that they are of negligible evolutionary importance if only for the reason that observations of sexual behaviour ..in general are extremely limited for wild ..siamang.. in part beca use of the typically long intervals between periods of fem ale receptivity" (Palombit 1994 p722).


2.6. REFERENCES Alcock, J (1993) Animal Behaviour (5th ed) Sunderland, MA: Sinauer Associates Birkhead, T & Moller, A.P (1996) Monogamy an d sperm competition. In Black, J.M (ed) Partnerships in Birds Oxford: Oxford University Press Burley, N (1981) Mate choice by multiple cri teria in a monogamous species American Naturalist 117, 515-528 Coolican , H (1990) Research Methods and Sta tistics in Psychology London: Hodder & Stoughton Gowaty, P.A (1996) Battle of sexes and origi ns of monogamy. In Black, J.M (ed) Partnerships in Birds Oxford: Oxford University Press Hill, G.E (1991) Plumage colouration is a se xually selected indicator of male quality Nature 350, 337-339 Hill, G.E (1992) Proximate basis of variatio n in carotenoid pigmentation in male house finches Auk 109, 1, 1-12 Hill, G.E et al (1994) Sexual selection and cuckoldry in a monogamous songbird: Implications for sexual selection theory Behavioural Ecology and Sociobiology 35, 193-199 Kleitman, D.G (1977) Monogamy in mammals Qua rterly Review of Biology 52, 39-69 Komers, P.E & Brotherton, P.N.M (1997) Femal e space use is the best predictor of monogamy in mammals Proceedings of the Royal Society of London B 264, 1261-1270 Kornerup, A & Wanscher, J.H (1983) Methuen H andbook of Colours London: Methuen Moller, A.P (1988) Female choice selects for male sexual trait ornaments in the monogamous swallow Nature 322, 640-642 Palombit, R.A (1994) Extra-pair copulations in a monogamous ape Animal Behaviour 47, 721-723 Reichard, U (1995) Extra-pair copulations in a monogamous gibbon (Hylobates lar) Ethology 100, 99-112 Trivers, R.L (1972) Parental investment and sexual selection. In Campbell, B (ed) Sexual Selection and the Descent o f Man Chicago: Aldine Williams, J.R et al (1994) Oxytocin administ ered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster) Journal of Neuroscience 6, 247-250 Young, L.J et al (1997) Species differences in V1a receptor gene expression in monogamous and non-monogamous voles: Behavioural consequences Behavioural Neuroscience 111, 599-605 Young, L.J et al (1998) Neuroendocrine basis of monogamy Trends in Neuroscience 21, 2, 71-75


3. ADVANTAGES AND DISADVANTAGES OF PARENTAL CARE AND INVESTMENT 3.1. Introduction 3.2. Prolonged parental care 3.3. Red deer and sex of offspring 3.4. References 3.1. INTRODUCTION The patterns of parental care (table 3.1) vary between species based on the amount of parental investment by each sex. "Investment" is seen as any thing done by a parent to increase the chances of the sur vival of that particular offspring, which is at the expen se of the parent's ability to invest in future offspring (Trivers 1972). Thus the parent who has invested mo re tends to care for that offspring, while the parent with the least investment may desert. � Both parents (biparental); � Female only; � Male only (sex role reversal); � No care - offspring left to fend for themselves imm ediately after

hatching or birth; � Alloparental care - care by individuals (usually ge netically

related) but not genetic parents; eg: eusocial inse cts; � Brood parasitism - fostering (care by genetic non-r elatives); ie:

placing eggs in nest unnoticed in case of cuckoo. Table 3.1 - Types of parental care. There are a number of parental care decisions and thus mating strategies (table 3.2). FEMALE STAYS FEMALE LEAVES AFTER BIRTH AFTER BIRTH MALE STAYS Equal investment Male greater inve stment than AFTER BIRTH by both partners; female; sex-role reversal monogamy MALE LEAVES Multiple partners Multiple partners for male; AFTER BIRTH for male; female many eggs must su rvive greater investment than male Table 3.2 - Different parental care decisions and m ating strategies. Maynard Smith (1977) viewed the relationship b etween


the parents as a "game" (as in "game theory") - an assessment of costs and benefits of staying or dese rting (table 3.3). AMOUNT OF FEMALE MORE MALE MORE THAN EQUAL INVESTMENT: THAN MALE FEMALE WHO CARES MALE FEMALE JOINT/BOTH FOR YOUNG: DESERT Table 3.3 - Strategies for parental care based on parental investment. The decision to desert or stay and care for th e offspring depends on a number of factors (Maynard S mith 1978): � Effectiveness of parental care by one vs two parent s. � The chances of the deserter being able to mate agai n. � The security of paternity for the male. � The age of the offspring. � Whether fertilisation is internal or external. Exte rnal

fertilisation in many species of fish, for example, leads to males care for the eggs (table 3.4).

FERTILISATION INTERNAL FERTILISATION EXT ERNAL MALE FEMALE BOTH MALE FEMALE BOTH 28 6 8 2 10 0 (After Breder and Rosen 1966) Table 3.4 - Number of species of bony fishes where different parents care for offspring based on type of fertilisation. 3.2. PROLONGED PARENTAL CARE In species that care for the young, that carin g stops when the offspring is a certain age (eg: fled gling that leaves the nest in birds). In many cases, the young leave the home in the process known as natal disper sion. But there are exceptions noted, particularly among birds, in the case of "co-operative breeding". This is whe re young from previous years aid the parents in raisin g this year's offspring through feeding or defence of the nest. Other species of birds, like swans, provide prolonged parental care (PPC) after the young can f eed themselves. The reason may include guiding the offs pring


on the first migration. Scott (1980) investigated PPC by Bewick's swan s (Cygnus columbianus bewickii)(figure 3.1) wintering at the Wildfowl Trust Refuge, Welney, Norfolk, UK. It has been suggested that PPC protects the offspring from aggression during feeding competition. Three predic tions were made based on this suggestion: 1. Cygnets should remain closer to parents in more crowded flocks; 2. Cygnets should remain closer to parents when fee ding on foods that produce aggressive encounters (eg: agricultural crops); 3. Cygnets of smaller body size and females will re main closer to parents.

(Source: Arpingstone; in public domain)

Figure 3.1 - Bewick's swans. Observations were made using point or focal sampling: "a sampling rota was developed in which, before each feed, five focal individuals were watched, eac h for 1 min every 10 min, such that A was watched for 1 m in,


then after a gap of 1 min, B was watched for 1 min and so on for C, D, and E and then A was found again" (p94 0). During that sample minute, all aspects of the birds interactions were recorded including distance to ma te, cygnet, or parents; and distance to three nearest unrelated neighbours. Event sampling was used for aggressive encounters (table 3.5).

Table 3.5 - Point and event sampling in observation s. Cygnets were significantly more successful in aggressive encounters when near parents (within 4 s wan lengths) than alone (75% vs 33% won; X² = 4.2; df = 1; p<0.05). Concerning the three predictions above: 1. Cygnets remained nearer to parents in more dense flocks (average 1.5m away vs 2.3m in less dense flo cks). 2. When the flock was eating waste potatoes that pr oduced more aggression, the cygnets remained approximately half as near to parents compared to feeding on winter wh eat where less aggression occurred. Mean relative dista nce of cygnet to parent was 1.0 for wheat and 0.6 for pota toes (p<0.05). 3. Females and smaller cygnets remained closer to parents. The cygnets were more confident closer to pare nts as shown by amount of time feeding: over 80% for those in close proximity compared to less than 40% when cygn et was seven or more swan lengths away. PPC meant that parents intervened in aggressiv e encounters on behalf of their cygnets (34% of encounters), and the presence of parents was enough in some cases to step aggression developing, especiall y with subordinate birds. But intervention had a cost for the parents, i f only to stop them feeding. For example, during October-November, parents spent under 60% of time feeding

POINT OR FOCAL SAMPLING EVENT SAMPLING

Description Record what individual is doing at point in time

Record details of an event every time it occurs

Advantage Record for all individuals being observed

Records key event as often as it happens

Disadvantage May miss information because focused on one individual at a time

Tends to look at the event out of context of other behaviour


compared to 80% for adult pairs without cygnets. The proximity changed over the winter period, however, and it was reduced by January-February (me an relative distance of 1.27 vs 0.72 in November-Decem ber). As the cygnets moved further away, the parents spen t more time feeding (80% of time in February-March). There were other beneficial changes in parents' behaviour over the winter (table 3.6).

Table 3.6 - Changes in two behaviours of parents ov er the winter. Any direct costs to parents, like reduced feed ing, while involved in PPC is compensated by "indirect fitness" in the survival of the offspring through f eeding or protection from aggression by unrelated adults. Table 3.7 summarises the main advantages and disadvantages of PPC.

Table 3.7 - Main advantages and disadvantages of PP C.

PARENTS PAIRS WITHOUT CYGNETS

SIG

Mean percentage of observations when adults alert (ie: heads up in vigilant position): Oct-Nov Dec-March

40 20

20 25

<0.05 ns

Threat frequency (per min) during feeding: Oct-Nov Dec-Feb

2.4 2.0

1.2 1.2

<0.02 ns


1. Indirect fitness with a greater chance of the offspring's survival and their production of offspring. 2. To teach offspring key survival skills like food sources and migration. 3. To protect offspring from predators and aggressive conspecifics (feeding competition). 4. The offspring benefit in terms of protection and feeding. 5. PPC means that offspring can still developed after birth/hatching.

1. Cost to parents in terms of less opportunity for feeding. 2. Cost to parents in terms of less opportunity for mating and further offspring. 3. Risk to parents in protecting offspring. 4. Offspring may not be able to fend for themselves when PPC ends. 5. Offspring that need PPC ca n be highly vulnerable in the first few days, weeks, and months.


3.3. RED DEER AND SEX OF OFFSPRING Parental investment in their young may vary depending on the sex of the offspring. For example, female red deer (Cervus elaphus) invest more in individual sons than individual daughters (Clutton- Brock et al 1981). This is shown in the red deer on the Scottish island of Rhum - male calves have significantly longer ges tation lengths (236.1 vs 234.2 days for females), signific antly heavier birth weight (6.72 vs 6.23kg), and suck fro m their mothers significantly more frequently (5.1 vs 2.6 daily suckling bouts). Also hinds who reared male c alves were less likely to produce a calf the following br eeding season, and those that did, gave birth later in the season compared to mothers of female calves (Clutto n-Brock et al 1981). Observations over twenty years on Rhum show a clear pattern between "maternal rank" and the production of male offspring. Maternal rank is defined as "the ratio of anim als which the subject threatened or displaced to animal s which threatened or displaced it weighted by the id entity of the animals displaced" (Clutton-Brock and Godfra y 1991) (table 3.8). MATERNAL RANK APPROXIMATE PERCE NTAGE OF OFFSPRING BORN MA LE low 0.1 20 0.3 30 0.5 45 0.8 65 high 1.0 75 (After Clutton-Brock et al 1986)

Table 3.8 - Correlation between "maternal rank" and percentage of male offspring born. The sex of the offspring in polygynous mammals is influenced by maternal conditions. Mothers in good conditions produce sons and those in poor condition s produce daughters. This is known as the Trivers-Wil lard hypothesis (Trivers and Willard 1973). The maternal conditions will be linked to the resources available to survive and raise the offspr ing. Where resources are plentiful, then the maximum gen es can be passed into future generations by male offspring based on grandchildren (figure 3.2). Daughters will alway s find a mate even if this limits the number of grandchild ren. The production of daughters is a better strategy wh ere


resources are limited. GOOD MATERNAL CONDITIONS POOR MATERNAL CON DITIONS MOTHER MOTHER ↓ ↓ MANY OFFSPRING ONE OFFSPRING ↓ ↓ SONS BETTER STRATEGY DAUGHTERS - ALWAY S FIND MATE ↓ ↓ ↓ ↓ GRANDCHILD GUARAN TEED FEMALE FEMALE FEMALE ↓ ↓ ↓ MANY GRANDCHILDREN FOR MOTHER DAUGHTERS GUARANTEED MATE, BUT = MORE GENES INTO FUTURE LIMITED GRANDCHIL DREN BUT SONS = RISK OF MANY MATINGS VS MAY NOT MATE Figure 3.2 - Different strategies for offspring in different maternal conditions. The dominance of the female will also influenc e the success of the offspring. High-ranking hinds produc e more sons because of the greater lifetime reproductive s uccess for those sons, and low-ranking hinds produce more daughters (Cockburn 1999). Work by Kruuk et al (1999) on Rhum island has noted that with increasing population density, high-ranki ng females produce more daughters. Increasing populati on density is an example of poor maternal conditions, and thus the production of daughters is a better evolut ionary strategy. However, Cockburn (1999) argues that male foet uses are more sensitive to resource availability, and mo re of them may be dying before birth with the increasing population density. The increase in female births i s in fact the increased survival of females at birth. It is unclear how the process of "choosing" th e sex of the offspring works. For example, the hormones f rom the mother could influence the production of girls, and testosterone from the fathers for boys. High social ranking males could have more testosterone and thus "determine" the sex of the offspring as male (Cartw right 2000). Maybe high-ranking hinds have more testoster one as well, and this explains the situation in red deer.


3.4. REFERENCES Breder, C & Rosen, D (1966) Modes of Reprodu ction in Fishes New York: Natural History Press Cartwright, J (2000) Evolution and Human Beh aviour Basingstoke: Macmillan Clutton-Brock, T.H & Godfray, C (1991) Paren tal investment. In Krebs, J.R & Davies, N.B (eds) Behavioural Ecology: An Evo lutionary Approach (3rd ed) Oxford: Blackwell Science Clutton-Brock, T.H et al (1981) Parental inv estment in male and female offspring in polygynous mammals Nature 289, 487-489 Clutton-Brock, T.H et al (1986) Great expect ations: Dominance, breeding success and offspring sex ratios in red de er Animal Behaviour 34, 460-471 Cockburn, A (1999) Deer destiny determined b y density Nature 399, 407-408 Kruuk, L.E.B et al (1999) Population density affects sex ratio variation in red deer Nature 399, 459-461 Maynard Smith, J (1977) Parental investment - a prospective analysis Animal Behaviour 25, 1-9 Maynard Smith, J (1978) The ecology of sex. In Krebs, J & Davies, N (eds) Behavioural Ecology: An Evolutionary Approach Oxford: Blackwell Scott, D.K (1980) Functional aspects of prol onged parental care in Bewick's swans Animal Behaviour 28, 938-952 Trivers, R (1972) Parent-offspring conflict American Zoologist 14, 249-264 Trivers, R & Willard, D (1973) Natural selec tion of parental ability to vary the sex ratio of offspring Science 179, 90-92


4. ADVANTAGES AND DISADVANTAGES OF LEK MATING 4.1. Introduction 4.2. Examples of lek behaviour 4.3. References 4.1. INTRODUCTION Lek polygyny is a specific type of polygamy wh ere males mate with multiple females. The male sets up a "symbolic territory" (a territory with little or no resources) in which to advertise himself in an area near to other leks, and females check out the options be fore mating with the best male. Good quality males get t o mate with many females, and females can mate only with t he best male (table 4.1). Parental care is solely the concern of females in such species.

Table 4.1 - Main advantages and disadvantages of le kking. When males establish their mating territory, resources are generally not important as in a "norm al" territory which is defended because of its resource s. The choice of a lekking site seems to be visibility to females; eg: Uganda kob (Kobus kob thomasi) choose areas with little vegetation (Wikelski et al 1996). 4.2. EXAMPLES OF LEK BEHAVIOUR Wikelski et al (1996) studied the marine iguan as


1. Convenient for females to assess all the males in one place and choose the best quality. 2. Works well in normally geographically dispersed species that come together at the breeding season only. 3. Good quality males get to mate with many females. 4. No costs to males of maintaining territory for long periods of time. 5. Females can mate in lek without being harassed by other males.

1. The system is open to exploitation by poor quality males who lurk near the best quality males and attempt forcible copulation. 2. Best quality males may run out of sperm for late-arriving females. 3. Risk of interference from males in neighbouring leks. 4. Problem of best quality males being temporarily monopolised by other females. 5. Females do not know if males with leks near centre are "honest signals" of good quality.


(Amblyrhynchus cristatus) on Genovesa island (Galáp agos archipelago, Ecuador). The mating season lasts from early December to early January, and three seasons were studied. Individual animals were marked by hot branding which left an identifiable mark while causing only superf icial skin damage. Four observers were trained for three days to aid inter-observer reliability. Observation took place during daylight hours by following a fixed route al ong the beach area. Focal (or point) observations were made at four locations, and all copulations were recorde d (behaviour sampling) 6. Three types of males were observed: � Territorial males who occupied and defended a

particular mating area for five consecutive days. T hey were larger than the other types of males. Females preferred to mate in territories because it avoided harassment from other males;

� Marginal males who did not occupy a territory and m oved

around attempting to forcefully mate with any femal es they mate;

� Sneaker males who were the size of females (smaller

than the average male) and who attempted to mate in territories where the territorial male was absent.

Females, who copulated only once per breeding season, preferred to mate with territorial males (t able 4.2), and with larger ones. Small territorial males were more successful if based close to large territorial males. Beehler and Foster (1988) called this the "h otspot phenomena" - small territorial males get "accidenta l matings" when near large territorial males.

(* = significantly different to other two; p = 0.01 ) (After Wikelski et al 1996)

Table 4.2 - Mating success of different types of ma le iguanas in the 1992-3 breeding season.

6 Focal or point sampling records what is happening at a particular moment in time, while behaviour sampling records every occasion of a particular behaviour.

TERRITORIAL MALES

MARGINAL MALES

SNEAKER MALES

Body mass (g) 657 503 424

Total copulations observed

129 6 6

Copulations per male 3.1* 0.4 0.3


A lek is like a "male beauty contest" for the females. Comparison is possible to aid the choice o f males. What are the characteristics of males that i mprove their mating success in this "beauty contest"? Many studies have looked at individual species using "vo te counting" (ie: number of matings) as success. Fiske et al (1998) sought to establish the general patterns of male mating success in leks using a "bare-bones" meta-an alysis (Hunter and Schnidt 1990) of forty-eight studies. Table 4.3 summarises the characteristics analy sed.

Table 4.3 - Characteristics of males that gain mati ng success in leks. Meta-analysis (Glass 1977) allows the "quantit ative summary of statistical tests from multiple studies" (Fiske et al 1998) by standardising the data (throu gh the effect size), and making general conclusions. Howev er, there are limitations to this technique (Fiske et a l 1998): i) Sample size of studies to use can be small; eg: nine studies on fighting frequency, and seven on ag e. ii) Dependent upon the studies performed. For example, fourteen of 27 species studied were birds, eight were amphibians, 2 were insects, and three mammals. iii) The "file drawer" problem. Significant re sults tend to get published, so it is not known how many non-significant studies were performed and not publishe d. Thus published studies may be unrepresentative of a ll the studies performed. Statistical techniques have been developed to overcome this problem (eg: number of s tudies needed to change effect size; Rosenthal 1979).

CHARACTERISTICS CONCLUSIONS (= mating success)

Attendance - time spent on lek Positive correlation: more time

Display frequency; eg: amount of time spent calling

Positive correlation: more time

Fighting frequency Positive correlation: more fighting

Location of territory Negative correlation: nearer lek centre

Size of territory No correlation

Male body size Weak positive correlation: larger body

Extravagant morphological traits; eg: antlers

Positive correlation: larger

Male age Positive correlation: older


iv) "Apples and oranges". This is the problem that meta-analysis combines studies that were measuring different things and in different ways. Female choice of mate depends upon "honest sig nals" of the male's quality. The usual signals are body s ize and plumage. One signal specific to lekking is the position of the territory towards the lek centre. Territories at the lek centre should belong to high-ranking males and/or those who are superior in abil ity to maintain such a territory if the signal is honest. The signal will not be honest if there is "queue-jumpin g". This is where fighting occurs, for example, and a l ower-ranked individual gains a higher rank by winning. Kokko et al (1998) investigated lek positions among black grouse (Tetrao tetrix)(figure 4.1) at sites i n central Finland over a eight-year period. The males at the centres tended to be superior in terms of fight ing and survival abilities. Queue-jumping tended not to happen often because of the risks of injury from fi ghts. The males queued for central lek territory (ie: wai ted until high-ranking males leave). It is an "evolutio nary stable strategy" (Maynard Smith 1982) - the best st rategy in terms of costs and benefits.

(Source: Gagea; in public domain)

Figure 4.1 - Black grouse in Sweden.


It is generally assumed that females will mate only once with the best quality male, but this is not al ways the case as with, for example, the ruff (Philomachu s pugnax). This shorebird has a genetic dimorphism in males; ie: two different males. One type has darker plumage and defends a "mating court" (1m²) during t he lekking season. The other is lighter and hangs arou nd the mating courts ("satellite behaviour")(Lank et al 20 02). Lank et al (2002) studied the mating behaviour of female ruffs (called "reeves") on a shoreline in Fi nland. About a quarter were observed to mate with more tha n one male on a single visit to the lek, and 17 of thirty -four broods had multiple fathers. Fourteen out of 23 ree ves observed mated with both types of males. Why do reeves mate with multiple males? The si mple answer is to diversify the genetics of the offsprin g. The costs for females of multiple matings are low becau se they do not risk the loss of paternal care as male support does not occur. "For whatever reason, a fem ale’s mating rule in many lekking species may be not the oft-stated search for the highest quality male, but rat her to seek several high quality mates" (Lank et al 2002 p 214). 4.3. REFERENCES Beehler, B.M & Foster, M.S (1988) Hotspots, hotspots and female preference in the organisation of lek mating strate gies American Naturalist 131, 203-219 Fiske, P et al (1998) Mating success in lekk ing males: A meta-analysis Behavioural Ecology 9, 4, 328-338 Glass, G.V (1977) Integrating findings: The meta-analysis of research Review of Research in Education 5, 351-379 Hunter, J.E & Schmidt, F.L (1990) Methods of Meta-Analysis: Correcting Error and Bias in Research Findings Newbury Park, CA: Sage Kokko, H et al (1998) Queuing for territory positions in the lekking black grouse (Tetrao tetrix) Behavioural Ecology 9, 4, 376-385 Lank, D.B et al (2002) High frequency of pol yandry in a lek mating system Behavioural Ecology 13, 2, 209-215 Maynard Smith, J (1982) Evolution and the Th eory of Games Cambridge: Cambridge University Press Rosenthal, R (1979) The "file-drawer problem " and tolerance for null results Psychological Bulletin 86, 638-641 Wikelski, M et al (1996) Lekking in marine i guanas: Female grouping and male reproductive strategies Animal Behaviour 52, 581-596


5. ADVANTAGES AND DISADVANTAGES OF NON-REPRODUCTIVE SEX IN ANIMALS 5.1. Post-conception mating 5.2. Homosexual interactions 5.3. References 5.1. POST-CONCEPTION MATING Sex is about reproduction among animals. Yet n on-reproductive sex exists, for example, by pregnant o r lactating females. What are the reasons for such behaviour, particularly among females (also known a s post-conception mating)? Table 5.1 lists the advant ages and disadvantages for males and females.

Table 5.1 - Advantages and disadvantages of non-reproductive sex. Stoinski et al (2009) observed one male gorill a with four females at the Zoo Atlanta in the USA. The gro up of five western lowland gorillas (Gorilla gorilla gorilla)(figure 5.1) were observed for a total of 2 73


MALES 1. Pleasure. 2. Strengthens the bond in monogamous species. 3. Male sexual competition.

1. Waste of sperm and cost of replenishing supply. 2. Energy costs of sex. 3. Risks of sexually transmitted disease.

FEMALES 1. To gain favour with dominant males. 2. To gain protection for self and offspring from dominant males. 3. To confuse males about paternity and gain support, and/or avoid infanticide. 4. Female sexual competition by reducing sperm of male available to other females. 5. Pleasure. 6. Strengthens the bond in monogamous species.

1. Risks of injury during sex. 2. Risks of sexually transmitted disease. 3. Does not confuse male about paternity if he knows that sex non-reproductive (eg: female shows signs of pregnancy). 4. Energy costs of sex.


hours over 245 days between December 2004 and Decem ber 2006. Females encouraging sex (solicitation) was de fined as "slowly approaching male with direct eye contact , often accompanied by pursued lips and attempts to t ouch the male" (p588).

(Source: Arpingstone; in public domain)

Figure 5.1 - Male gorilla. Non-reproductive females offered sex when othe r females were sexually active (table 5.2).

(After Stoinski et al 2009)

Table 5.2 - Solicitations by four female gorillas.

TOTAL SOLICITATIONS

KUCHI KUDZOO SUKARI LULU

Single occurrence days - only one female sexually active

36 17 6 3 10

Co-occurrence days - another female sexually active

75 20 9 17 29

Significance <0.05 ns <0.05 <0.01 <0.01


It seemed to be a case of if they are doing it , I better do it too. For the non-reproductive females, offering sex could have been to gain favour and protection of the self and offspring from the male, or to stop the male copulating with the reproductive fema les by depleting his sperm. When there is more than one male, non-reproduc tive sex by the female is a way of confusing the male ab out paternity, and thereby encouraging him to care for her and her offspring. 5.2. HOMOSEXUAL INTERACTIONS A different aspect to non-reproductive sex is where same-sex individuals court and attempt to mate - "homosexual interactions" (Maklakov and Bonduriansk y 2009). Such behaviour may assert dominance over riv als, or be practice for heterosexual encounters. More generally, it is felt to be a perceptual error (or lack of sex recognition). For example, male water bugs (Palmacorixa nana) mount any individual large than themselves because females are generally larger tha n males (Aiken 1981). Maklakov and Bonduriansky (2009) investigated homosexual interactions in two species of insects: � Carrion fly (Prochyliza xanthostoma) - Males fight over

territories from which females are courted with a "dance". The cost of homosexual interactions are en ergy loss through the "dance" and injury during fights;

� Seed beetle (Callosobruchus maculatus) - Males chas e

females and mount without courtship. Sex is dangero us for females as the penis has spines attached. The c ost of homosexual interactions would be loss of energy and water, and fatal injury as the mounting male's genitalia can get stuck under the elytra (hardened forewings) of another male.

The cost of homosexual interactions were measu red in terms of deaths in six experimental conditions - ma les and females alone, all male and all female groups, and males and females in mixed sex groups. In both spec ies, males in all male groups had shorter lifespans. In terms of evolution, male homosexual mountin g in insects is the product of the benefits of rapid, indiscriminate mating over the costs of discriminat ing males from females (Thornhill and Alcock 1983). As long as the former is greater, then there is no need for the evolution of mechanisms to identify same sex.


5.3. REFERENCES Aiken, R.B (1981) The relationship between b ody-weight and homosexual mounting in Palmacorixa nana Walley (Heteroptera: C orixidae) Florida Entomologist 64, 267-271 Maklakov, A.M & Bonduriansky, R (2009) Sex d ifferences in survival costs of homosexual and heterosexual interactions: Evidence from a fly and a beetle Animal Behaviour 77, 6, 1375-1379 Stoinski, T.S et al (2009) Sexual behaviour in female western lowland gorillas (Gorilla gorilla gorilla): Evidence for se xual competition American Journal of Primatology 71, 7, 587-593 Thornhill, R & Alcock, J (1983) The Evolutio n of Insect Mating Systems Cambridge, MA: Harvard University Press

Animal Behaviour Advantages Disadvantages No2

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