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Kevin Brewer

ISBN: 978-1-904542-47-6
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Kevin Brewer BSocSc, MSc


An independent academic psychologist, based in England,

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,
RM16 3EW

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 2
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

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 3
1.1. Introduction
1.2. Avoiding inbreeding
1.3. Adaptations with inbreeding
1.4. Amur leopards
1.5. References


Inbreeding refers to matings among genetic relatives

that reduces the variety of genes (an increase of
homozygosity). "This could eventually lead to a
'mutational meltdown' for populations with an effective
size ..of <100" (Keller and Waller 2002 p230). Inbreeding
can be defined in a number of ways (Keller and Waller

 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 degree of

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

 Inbreeding because of population subdivision - Small

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 depression"
(Keller and Waller 2002). For example, a higher rate of
parasites and this reduced survival over winter in Soay
sheep (Ovis aries) on a Scottish island (Coltman et al
Crnokrak and Roff (1999) found statistically
significant levels of inbreeding depression in 54% of
species known to be inbred.

Keller (1998) analysed the inbreeding coefficient of

song sparrows on a Canadian island to quantify the

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 4
reduction in fitness. A mating between first degree
relatives (eg: mother-son) reduced the hatching rate by
around one-half, and this became three-quarters with two
generations of such matings.
While among baboons where males mate with females in
natal troops (close genetic relatives including
siblings), infant mortality was 100% in two studies, but
none at al in another (table 1.1).


Olive baboon 4/4 inbred vs 6/32 Packer (1979)
(Papio anubis)(figure outbred infants died in
1.1) first month
Yellow baboon 3/3 inbred vs 27/140 Alberta and
(Papio cynocephalus) outbred infants died in Altmann (1995)
first month
Chacma baboon No difference in Bulger and
(Papio cynocephalus mortality between Hamilton (1988)
ursinus) inbred and outbred
infants up to three
months old

(After Pusey and Wolf 1996)

Table 1.1 - Three studies of baboon inbreeding and infant


(Source: US Fish and Wildlife Service; public domain)

Figure 1.1 - Olive baboon.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 5
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).


 Clutch/brood size  Juvenile  Number of clutches
 Nestling survival survivorship  Clutch size
 Number of eggs  Probability of  Hatching success
hatched producing litter  Number of dead
 Number of young  Litter size embryos
fledged  Juvenile weight  Percentage fry
 Hatching success  Number of emergent survival
young  Growth of adults
 Percentage of
emergent young
 Ejaculation volume
 Sperm motility
 Body mass

Table 1.2 - Criteria used to measure the effect of

inbreeding in different species.

Table 1.3 gives examples of studies showing effects

of inbreeding in different animals.


Blue tit Reduced hatching rate Kempenaers et al
(Cyanistes caeruleus) (1996)
Common shrew Survival to maturity; Stockley et al (1993)
(Sorex araneus) body length
Harbour seal Birth weight; Coltman et al (1998)
(Phoca vitulina) neonatal survival
Black-footed rock Fecundity (ie: amount Eldridge et al (1999)
wallaby of offspring)
(Petrogale lateralis)

(After Keller and Walter 2002)

Table 1.3 - Examples of studies on effect of inbreeding

in a population.

Table 1.4 gives some examples of studies showing

specific inbreeding relationships in different animals.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 6
Golden lion Father- 14/14 inbred vs 1/5 Dietz and
tamarin daughter; outbred infants Baker (1993)
(Leonpithecus siblings died before weaning
Cooper's hawk Grandmother- Low hatching rate Rosenfield
(Accipiter grandson and
cooperii) Bielefeldt
White-footed Siblings Lower survival rate Jiménez et al
mice when individuals (1994)
(Peromyscus born in captivity
leucopus released into wild

(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.

Allele is a possible copy of a gene at a particular point of the chromosome.
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 7

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 eusocial species, like

ants, inbreeding is very high because only one female and a limited
number of males mate. Among naked mole-rats (Heterocephalus
glaber)(figure 1.3), that live in subterranean colonies in north-east
Africa, "DNA fingerprinting" showed a mean relatedness 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 caring 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 barriers to
movement (Reeve et al 1990).

4. Risks of outbreeding including genetic incompatibility, 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 genetically similar mates
(Box 1.1).


1. Inbreeding depression; ie: reduced evolutionary fitness including

sperm deformities, sterility, and decline in courtship frequency
(Pusey and Wolf 1996).

2. Greater chance of young not surviving to adulthood; eg: inbred

red-cockaded woodpeckers (Picoides borealis) in south-eastern USA
have reduced hatching rates and fledgling survival (Daniels and
Walters 2000).

3. Increased extinction risk, particularly for small populations,

through reduced survival of young and shorter lifespan 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 novaboracensis) over ten weeks
after introduction to the wild at fields near Chicago Zoological
Park, Brookfield, Illinois, USA. On average, survival of inbred mice
was 56% that of non-inbred ones, mainly due to a greater loss of body
mass by the former group.

5. Greater susceptibility to changes in the environment; eg: more

inbred song sparrows (Melospiza melodia) died during storms on
Mandarte Island, Canada (Keller et al 1994).

Table 1.5 - Advantages and disadvantages of inbreeding.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 8
(Source: Ltshears - Trisha M Shears; public domain)

Figure 1.3 - A naked mole-rat.

Great frigatebirds (figure 1.4) breed on remote islands 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 twelve
small islands in the French Frigate Shoals atoll,
northwestern Hawaiian islands, USA), where the population
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 for DNA

fingerprinting from 92 family groups in 1998 and 1999.
Genetic similarity between mates was greater than expected
by chance (mean relatedness of 0.082; significantly
different to zero) suggesting inbreeding. The authors
concluded: "Although the potential for fitness
consequences of this inbreeding remains unclear, the
occurrence of inbreeding in this population is intriguing
because it is likely to be the result of a active mate
choice process" (p1234).

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

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 9
(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 between

incestuous and non-incestuous mating;

b) Sequential choice scenario - Choice between

mating with kin now or waiting for non-kin to appear.

In the second situation, waiting for non-kin is

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, inbreeding
can make sense for the parent who cares for the
offspring. A female who has a period of pregnancy and
after-birth care is not able to mate again for a while.
This is a "time out" (Kokko and Ots 2006). If such a
female has mated with a related male, who then mates with
unrelated females, she has gained indirect fitness from
inbreeding. Indirect fitness refers to benefits at the
level of the gene.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 10

1. One way of avoiding inbreeding is through natal

dispersion. At a certain time, juveniles are sent or
choose to leave their group or site of birth.

For example, male and female juvenile meadow voles

(Microtus pennsylvanicus) were found to be more likely to
disperse when released into a empty area with siblings
than with non-siblings (Bollinger et al 1993).

But dispersal has costs including predation risk,

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, female
white-footed mice preferred to mate with unfamiliar first
cousins than unfamiliar siblings or unfamiliar unrelated
males (Keane 1990), and similarly Japanese quail females
(Bateson 1982).

Ekernas and Cords (2007) studied natal dispersion at

between 6-8 years-old by young male blue monkeys
(Cercopithecus mitis stuhlmanni) in the Kakamaga Forest,
Kenya. Twenty-six natal dispersions were observed among
three studied groups (each group ranging from thirty-
three to sixty-five individuals).
Four factors were analysed to explain the dispersal

i) Dispersed males hounded out by adult males - This

did not seem to be important as there was no difference
in aggressive encounters between adult males and
individuals who subsequently did or did not leave the

ii) Dispersed males did not have mating

opportunities - If this was the case, dispersion would
occur during the mating season, and it did not more often
than expected by chance.

iii) Dispersed males have weaker social ties to 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 dispersal

was more often during the dry season, and least likely
when food was scarce. This would suggest that dispersion
took place when the movers had a better chance of being
accepted by the new group (ie: not during food

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 11
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).


May-Sept Most 7 ns
Dec-Feb Lowest average 16 more; p<0.0001
June-August Food shortages 1 ns

Table 1.6 - Distribution of dispersals in three seasons.

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 the

female socially dominated "clans". Höner et al (2007)
analysed ten years of data on the hyena population of
Ngorongoro Crater, Tanzania (370 individuals in eight
clans), and found 90% of males dispersed.
Females mate with several males which means that
female offspring may not be able to recognise their
genetic father, so they follow the rule: "avoid males
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 into the
female's group after her birth. Only two litters (of 309)
were cubs from daughter-father matings.

2. Another way to overcome the risk of inbreeding is

female extra-pair copulations with males from outside the
natal group.

For example, splendid fairy wrens (Malurus

splendens) were estimated to have breeding pairs with
close relatives in 25% of cases (compared to the average
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


Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 12
Experiments place related individuals together or
unrelated individuals to measure reproductive rates,
which are lower among the related group, or individuals
are offered a choice of mates of varying genetic
relatedness. For example, wild house mice (Mus musculus)
in sibling groups were less likely to produce litters
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 close

relatives; eg: marmosets and tamarins in the presence of
opposite sex parents and siblings in their group.


In animals that show inbreeding, their behaviour may

be different with kin - for example, ejaculating less
sperm. Lewis and Wedell (2009) found that Indian meal
moth (Plodia interpunctella)(figure 1.5) males ejaculated
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 different
fertile and non-fertile sperm. Sisters received
significantly less fertile and non-fertile sperm (table


Fertile 3000 4000
Non-fertile 30 000 45 000

Table 1.7 - Approximate mean number of sperm provided to

unrelated and related females.

Sperm production is costly for male moths who can

mate only a handful of times (maximum eight; Ryne et al
2001) in their short lives (12 days average). Males also
vary their ejaculation depending on the quality/fecundity
of the female, and the presence of other males (sperm
competition)(Lewis and Wedell 2009).
But in red junglefowl (Gallus gallus), Pizzari et al
(2004) found that males inseminated sisters with more
sperm that unrelated females. This was because females
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 inbreeding
(Tregenza and Wedell 2002).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 13
(Source: Kaldari; in public domain)

Figure 1.5 - Indian meal moth.


The Amur (or Far Eastern) leopard (Panthera pardus

orientalis) may be reduced to less forty wild individuals
alive in the Russian Far East (Uphyrkina et al 2002).
When a population is small the opportunities for
breeding are limited, and this can lead to mating with
close genetic relatives Inbreeding). Inbreeding increases
the risk of recessive genes (those needing both copies of
the gene to manifest the effect) and congenital problems

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 14
(eg: bone deformity). Also a decrease in litter size has
been reported by field researchers (from two in 1973 to
one in 1997)(Uphyrkina and O'Brien 2003).
Uphyrkina and O'Brien (2003) found that wild Amur
leopards from the Primorskiy Kray area of Russia and
North Korea showed lower genetic variation than captive
populations from zoos worldwide, and relatedness values
of between 60-90% 2.
The documentary, "The Last Leopard" (Director:
Tatsuhiko Kobayashi), filmed Amur leopards in Kedrovaya
Pad Natural Reserve, west of Vladivostok, Russia. The
documentary reported genetic analysis of seven animals
which showed inbreeding (figure 1.6).

Figure 1.6 - Genetic relationship between seven Amur

leopards in Kedrovaya Pad Natural Reserve.

100% = identical twins; 50% = parent-offspring and between siblings.
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 15
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 with 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 (Skrytnaya).
Half-siblings normally share 25% of the same gene (and
full siblings 50%). The coefficient of inbreeding is
12.5% here.

(iv) Inbreeding. The father (Puzan) mates with his

daughter (Skrytnaya) to produce cub 3.

Abbott, D.H (1993) Social conflict and reproductive suppression in
marmoset and tamarin monkeys. In Mason, W.A & Mendoza, S.P (eds) Primate
Social Conflict New York: State University of New York Press

Alberta, S.C & Altmann, J (1995) Balancing costs 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 avoidance 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 ursinus population Animal
Behaviour 36, 574-578

Cohen, L.B & Dearborn, D.C (2004) Great frigatebirds, Fregate minor,
choose mates that are genetically similar Animal Behaviour 68, 1229-1236

Coltman, D.W et al (1998) Birth weight and neonatal survival of

harbour seal pups are positively correlated with genetic 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 Evolution 53, 1259-1267

Crnokrak, P & Roff, D.A (1999) Inbreeding depression in the wild

Hereditary 83, 260-270

Daniels, S.J & Walters, J.R (2000) Inbreeding depression and its

Details of conservation efforts at and http://www.amur-
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 16
effects on natal dispersion in red-cockaded woodpeckers 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 rosalia Animal Behaviour
46, 1067-1078

Ekernas, L.S & Cords, M (2007) Social and environmental factors

influencing natal dispersal in blue monkeys, Cercopithecus mitis stuhlmanni
Animal Behaviour 73, 1009-1020

Eldridge, M.D.B et al (1999) Unprecedented low levels of genetic

variation and inbreeding depression in an island population of the black-
footed rock wallaby Conservation Biology 13, 531-541

Höner, O.P et al (2007) Female mate-choice drives the evolution of

male-biased dispersal in a social mammal Nature 448, 798-801

Jiménez, J.A et al (1994) An experimental study 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 leucopus Animal Behaviour
39, 264-273

Keller, L.F (1998) Inbreeding and its fitness effects in an insular

population of song sparrows (Melospiza melodia) Evolution 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 inbred song sparrows during

a natural population bottleneck Nature 372, 356-357

Kempenaers, B et al (1996) Genetic similarity, 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 inbreeding 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 reproduction test Ethology
88, 99-108

Lewis, Z & Wedell, N (2009) Male moths reduce sperm investment in

relatives Animal Behaviour 77, 6, 1547-1550

Packer, C (1979) Inter-troop transfer and inbreeding avoidance in

Papio anubis Animal Behaviour 27, 1-36

Pizzari, T et al (2004) Sex specific, counteracting responses to

inbreeding in a bird Proceedings of Royal Society of London, Series B 271,

Pusey, A & Wolf, M (1996) Inbreeding avoidance in animals Trends in

Ecology and Evolution 11, 5, 201-206

Ralls, K et al (1988) Estimates of lethal equivalents 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-rat 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

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 17
Natural History of Inbreeding and Outbreeding: Theoretical 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 the Indian male moth
Behaviour 138, 947-963

Stockley, P et al (1993) Female multiple mating behaviour in the

common shrew as a strategy to reduce inbreeding Proceedings of the Royal
Society of London B, Biological Sciences 254, 173-179

Tregenza, T & Wedell, N (2002) Polyandrous females 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 genetics of the Far Eastern

leopard (Panthera pardus orientalis) Journal of Hereditary 93, 5, 303-311
(Freely available at

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 18
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


Monogamy involves mating (and often parental care)

by one male and one female for a breeding season or for
life. It is the form of social organisation found in
about 3% of mammals (Young et al 1998), but in 15% of
primates (Reichard 1995).
The alternatives are polygamy (mating with multiple
individuals who help in caring for the young), or
promiscuity, which is multiple-partner matings without
any post-copulation relationship. The best strategy will
also vary between males and females (table 2.1).


1. Monogamy: one partner for breeding season

a. Mate-assistance monogamy Male assists female

in child-rearing

b. Mate-guarding monogamy Female dispersal

2. Polygyny: one male with multiple females

a. Female defence polygyny Male defends cluster

of females

b. Resource defence polygyny Male defends

resources and females

c. Lek polygyny Male defends

territory and females
come to mate only

d. Scramble competition polygyny Males find scattered



1. Monogamy

a. Female-enforced monogamy Male keeps other

females away and
assists in child-

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 19
2. Polyandry: one female with multiple males

a. Fertility-insurance polyandry Greater fertilisation

of eggs

b. Better sperm polyandry Genetically diverse


c. More material benefits polyandry More resources from


d. More paternal care polyandry More males help in

(After Alcock 1993)

Table 2.1 - Types of mating strategy.

The best strategy for passing the genes into the

next generation will vary between the male and female of
the species. The male is able to produce many sperm, and
so can theoretically have as many offspring as mates
But the female is restricted, in most species, by
giving birth to the offspring. Thus she has more invested
in its survival (table 2.2).

Different species behave in different ways depending

upon their environments, but generally the example in
table 2.2 is the common strategy of sexual selection.
"Female choosiness" has led to the evolution of males who
compete, in some way, to show the female that their genes
are best for mating. This competition involves fights,
"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 have

one offspring each in the breeding season


MALE 10 fathered; can Find many female mates; ie:

afford some not indiscriminate; little concern
to survive for post-natal care

FEMALE Each female has Female invests time and effort

one offspring in survival, but must exercise
and thus survival choosiness about male; ie: only
important mate with male who has "best

Table 2.2 - Sexual selection and strategies for males and


Table 2.3 shows the factors that influence mating

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 20



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 eg 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.


There are different types and explanations of

monogamy including obligate and facultative (Kleitman
1977). The former relates to the need of the offspring to
be cared for by both parents. Facultative monogamy is
where males cannot monopolise more than one female
because the females are geographically dispersed (Komers
and Brotherton 1997).

Komers and Brotherton (1997) compared these two

types of monogamy in different mammal species. "Paternal
care was considered to be present if males of that
species are known to retrieve young, transport young, or
provide food" (p1261).
Monogamy was found to exist significantly more often
in the absence of parental care than in the presence of
it. "For a general theory on the evolution of monogamy in
mammals, we must therefore focus on factors other than
paternal care that may have promoted monogamy" (Komers
and Brotherton 1997 p1267). Monogamy was also not common
in species with geographically dispersed females, but it
was more common where females were solitary living in
small, exclusive territories that males could monopolise.
Staying with one female reduced the risk and costs for

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 21
males of searching for multiple females.
Table 2.4 summarises the main advantages and
disadvantages of monogamy.


1. Know quality of partner and their genes.

2. Usually help with rearing young, which is crucial when biparental

care is required.

3. Less risk of female-female and male-male aggression compared to


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 geographically dispersed

and/or scarce.

7. Males can be certainty of their paternity compared to polyandry.


1. Fear of extra-pair copulations, and males, in particular, 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 will be


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 season, particularly

for males, compared to polygamy.

Table 2.4 - Advantages and disadvantages of monogamy.

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 genes
(table 2.5).

1. Ensures pairing with the right species

2. Permits survival in aggressive species; ie: to approach
without being attacked
3. Display of fitness
4. Improves species; ie: only fittest survive
Table 2.5 - Functions of courtship.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 22
Potential mates have to "establish clues to species
identification, genetic superiority, and complementarity
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 criteria
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 pattern

("checker" or "bar");

ii) Age and reproductive experience - "Super-

experienced (eight or more clutches), "semi-experienced
(1-2 clutches), or "no experience. (Experience leads 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 rank.

The preference for these different characteristics

was tested by giving a pigeon ("chooser") a choice of two
opposite-sex birds with differences in specific ways.
Table 2.6 summarises the findings in the choice tests.


Plumage Blue over ash-red Blue checker over blue bar;
blue bar over ash-red bar or
Age and More experienced; More experienced; experience
experience experience more more important than age; Less
important than age; experienced young over super-
Less experienced young experienced old
over super-experienced
Dominance No preferences Experienced females preferred
dominant males; inexperienced
females no preference

Table 2.6 - Preferences by pigeons on choices of

individual characteristics.

All the individual preferences were combined into a

selectivity index, which showed that females were more
selective than males. This fits with the prediction that
the sex who makes the greater parental investment will be
more selective (Trivers 1972); ie: females in monogamy.
However, Burley (1981) admitted that selectivity is

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 23
not necessarily constant over time, and may vary with
length of time since heterosexual contact, and season.
For example, with the latter, males had stronger
preferences in August-October than in January-March.


The vole of North America is interesting to study in

relation to social organisation because different species
show completely different behaviours. The prairie vole
(Microtus ochrogaster)(figure 2.1) is monogamous, while
the montane vole (Microtus montanus) is promiscuous
(table 2.7).


Mating Monogamy Promiscuous
Parental Both parents involved in Mother only, but even she
care prolonged care of abandons young soon after
offspring birth
Behaviour High level of social Low level of social contact
contact as species (50% (5% of time). Live in
of time in contact in isolated burrows.
experiments). Paired
males aggressive towards
other members of species

Table 2.7 - Differences in social organisation between

two species of voles.

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

Figure 2.1 - Prairie vole.

The difference between the two species of voles has

been explained by the hormones, oxytocin and vasopressin.
Oxytocin triggers maternal behaviour, and partner
preference in female prairie voles. While vasopressin
triggers paternal care, and partner preference in male
prairie voles (Young et al 1998).
Research has shown that in prairie voles copulation
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 24
triggers oxytocin release because where it is blocked by
drugs, the female does not stay with the male after
mating (Williams et al 1994). The prairie vole brain 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 1998).
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 increased
autogrooming only (Young et al 1997).


Sexual selection explains the different strategies

by males and females of a species when looking for a
mating partner. For example, female choosiness leads to
the evolution of males who can display their good quality
genes in obvious ways, like the strength of calls or
visual "ornaments", or males who provide resources to
support the female during pregnancy and after birth.
In a polygynous system, where females mate with
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 not
breed. However, female extra-pair copulation (EPC) widens
the choice of genes, particularly if the male breeding
partner has low quality genes (Hill et al 1994). So males
need still to signal their quality of genes. For example,
male barn swallows with longer tail streamers (signal of
good genes) engage in more EPCs than short-tailed males
(Moller 1988).

Where male care is essential, this will influence

females from seeking EPCs (figure 2.2).


↓ ↓

↓ ↓

↑ ↑
(After Birkhead and Moller 1996)

Figure 2.2 - Females seeking extra-pair copulations.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 25
Hill et al (1994) investigated female EPC among
house finches (Carpodacus mexicanus)(figure 2.3) in one
breeding season (1991) at the University of Michigan, Ann
Arbor, USA. The bright plumage of the males is an "honest
signal" of gene quality and parental investment. Males
with brighter plumage have been observed to feed
incubating females more than males with dimmer plumage
(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 underside,
crown, eyestripe, and rump) to give a single index of
overall plumage brightness. Blood samples were also taken
for "DNA fingerprinting" to establish paternity. Broods
from thirty-five nests were analysed (n = 119 chicks). 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 cuckolded and
non-cuckolded males. The results were not as expected,
and the only variable showing a significant difference

The plumage colour varies from pale yellow to bright red (Hill 1992).
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 26
was nest dispersion - all illegitimate nestlings were in
closely dispersed nests.
If there is no difference in plumage brightness and
cuckoldry, the authors asked, why would bright plumage
evolve in male house finches. One answer is that there
are more males than females (sex ratio of 1.52 males to
one female), and so males are competing to find a mate.
Also brighter plumage males mate earlier in the breeding
season (by as much as 100 days at the extremes), and 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 bands 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 based

on adding 21 individual scores together - seven regions
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). The
reliability of such a score could be open to question.

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 potentially

important in a study of paternity. If a female or her
mate is detained during the female's fertile period,
observer-induced EPCs may result. Most birds in this
study were sampled before the start of nest-building or
after egg-laying was complete when handling should not
have affected paternity. However, a few males and females
were just captured just prior to or during egg-laying, so
we also looked for an effect of capture date on

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).
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 27
cuckoldry" (Hill et al 1994 p194).

5. Standard procedures of the time were used for "DNA

fingerprinting" and thus calculating paternity. However,
the cost of the process was high and this limited the
sample size of the study.

6. One-tailed tests were used for statistical analysis as

a clear prediction of duller plumage males experiencing
more cuckolds was made (one-tailed research hypothesis).
One-tailed tests have less risk of a Type I error
(claiming a significant result when the findings were due
to chance; ie: non-significant).

7. The differences between cuckolded and non-cuckolded

males were statistically analysed with the Mann-Whitney U
test (table 2.8). This test was used because the plumage
brightness index score can be classed as ordinal data,
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).


Plumage 62 0.44 5, 26 27
brightness score
Wing length 40.5 0.11 5, 25 27
Female plumage 29.5 0.30 5, 17 17
Clutch initiation 55 0.59 5, 26 27
Clutch size 41.5 0.30 5, 23 24
Male age 56 0.31 5, 26 27

(* = 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 Whitney

tests comparing cuckolded and non-cuckolded males.

1. Does not need groups to be of 1. Not as efficient as parametric
equal size. tests.

2. Good with small samples. 2. Deals with relative positions

not absolute scores.
3. Not restricted by parametric
criteria. 3. Problems if too many tied

Table 2.9 - Main advantages and disadvantages of the Mann

Whitney U test.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 28
8. The sample size of cuckolded males was low (n = 5)
which could mean that there is low statistical power in
the statistical analysis. This means that the statistical
test is limited in its ability to find a significant
difference in the data.

9. The means of the plumage brightness scores were used,

whereas the median may have been better (table 2.10).

Definition Add up scores and divide Put data into order and
by number of scores. take middle number.
Advantages 1. Most sensitive 1. Shows exact middle
measure of central point with 50%
tendency. above/below.

2. Total and all values 2. Unaffected by extreme

taken into account. values in one direction.
Disadvantages 1. Not good if extreme 1. Less information used
scores or scores vary than the mean.
greatly as with small
samples. 2. Time consuming to
rank large sets of data.
2. Not good with highly
skewed distributions.

Table 2.10 - Mean and median as measures of central


10. The differences were presented graphically with box-

plots, which show the distribution of the scores with
10th, 25th, 50th, 75th and 90th percentiles. However,
this can be distorted by the small number of cuckolded
males (table 2.11).



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.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 29

Reichard (1995) reported EPCs among three families

of white-handed gibbons (Hylobates lar)(figure 2.5)
observed in Khao Yai National Park,Thailand (table 2.12).


A 4 Fearless Andromeda
B 5 Bard Bridget
C 6 Cassius Cassandra

Table 2.12- Details of three family groups observed by

Reichard (1995).

(Source: Ltshears)
Figure 2.5 - White-handed gibbon.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 30
Among these long-term monogamous primates, observed
daily for nearly eighteen months between January 1992 to
August 1993, three EPCs were witnessed: Andromeda and
Cassius twice, and Andromeda and Bard. Reichard's field
notes described the last occasion thus: " [0645h]
Immediately, a copulation in a dorso-ventral position
followed. It lasted only a few seconds, because
[Fearless] - who probably detected the EPC - charged
towards the couple and vigorously pursued the escaping
[Bard] for more than 30 minutes" (p106).

The EPCs were only 12% of all copulations observed

by Reichard (1995), the majority were with the paired
male (76 of 82). Though the female may gain other genes
from an EPC, there is a risk of injury in the activity
and her partner may then seek EPCs (table 2.13). The
evolutionary response to female EPCs for males is mate-
guarding and retention behaviour.

1. To gain better genes. 1. Risk that male partner will
engage in EPC.
2. To gain a variety of genes,
particularly if inbreeding 2. Risk that partner may leave
involved. offspring (mate desertion).

3. To increase sperm competition 3. Risk of injury during EPC.

and consequently reproductive
rate. 4. Risk of injury from mate.

4. To lower the risk of 5. Risk of diseases and

infanticide if EPC male becomes pathogens.

5. The fear of EPC can encourage

the mate to copulate more, and
mate-guarding behaviour.

Table 2.13 - Advantages and disadvantages of EPCs for

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 can be
converted into quantitative data later). This type of
study has advantages and disadvantages (table 2.14).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 31
1. Very detailed study of gibbons 1. Depends upon the observer; ie:
over long periods of time. information may be missed because
of the focus on one event or that
2. All observations are recorded it takes place outside the
for later analysis. observer's field of view.

3. The observer is able to 2. The animals were well

recognise individual animals and habituated to human observers,
record their behaviour. but does the presence of such
observers change the gibbons'

3. Very time consuming for the


Table 2.14 - Advantages and disadvantages of Reichard'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 of EPC.
These involved a female siamang mating with three males
from a neighbouring group at different times (table


Immature male of P group (3 15 February 1986
times) 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

Table 2.15- Five EPCs by female siamang from C group.

The "C" female "played a role in initiating them 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.. 'solicitation'
gesture at some extra-group males.." (p722). This female
may have been motivated to find EPCs because she produced
a premature stillborn and no other offspring during the

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 32
(Source: Vassil; in public domain)

Figure 2.6 - Siamang.

In both this study and Reichard (1995), the EPCs

were rare, but it does not mean "that they are of
negligible evolutionary importance if only for the reason
that observations of sexual behaviour general are
extremely limited for wild ..siamang.. in part because of
the typically long intervals between periods of female
receptivity" (Palombit 1994 p722).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 33
Alcock, J (1993) Animal Behaviour (5th ed) Sunderland, MA: Sinauer

Birkhead, T & Moller, A.P (1996) Monogamy and sperm competition. In

Black, J.M (ed) Partnerships in Birds Oxford: Oxford University Press

Burley, N (1981) Mate choice by multiple criteria in a monogamous

species American Naturalist 117, 515-528

Coolican , H (1990) Research Methods and Statistics in Psychology

London: Hodder & Stoughton

Gowaty, P.A (1996) Battle of sexes and origins of monogamy. In Black,

J.M (ed) Partnerships in Birds Oxford: Oxford University Press

Hill, G.E (1991) Plumage colouration is a sexually selected indicator

of male quality Nature 350, 337-339

Hill, G.E (1992) Proximate basis of variation 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 Quarterly Review of Biology

52, 39-69

Komers, P.E & Brotherton, P.N.M (1997) Female 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 Handbook 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 of Man Chicago: Aldine

Williams, J.R et al (1994) Oxytocin administered 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

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ISBN: 978-1-904542-47-6 34
3.1. Introduction
3.2. Prolonged parental care
3.3. Red deer and sex of offspring
3.4. References


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 anything
done by a parent to increase the chances of the survival
of that particular offspring, which is at the expense of
the parent's ability to invest in future offspring
(Trivers 1972). Thus the parent who has invested more
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 immediately after
hatching or birth;
 Alloparental care - care by individuals (usually genetically
related) but not genetic parents; eg: eusocial insects;
 Brood parasitism - fostering (care by genetic non-relatives); 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).



MALE STAYS Equal investment Male greater investment than

AFTER BIRTH by both partners; female; sex-role reversal

MALE LEAVES Multiple partners Multiple partners for male;

AFTER BIRTH for male; female many eggs must survive
greater investment
than male

Table 3.2 - Different parental care decisions and mating


Maynard Smith (1977) viewed the relationship between

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 35
the parents as a "game" (as in "game theory") - an
assessment of costs and benefits of staying or deserting
(table 3.3).





Table 3.3 - Strategies for parental care based on

parental investment.

The decision to desert or stay and care for the

offspring depends on a number of factors (Maynard Smith

 Effectiveness of parental care by one vs two parents.

 The chances of the deserter being able to mate again.

 The security of paternity for the male.

 The age of the offspring.

 Whether fertilisation is internal or external. External

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


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


In species that care for the young, that caring

stops when the offspring is a certain age (eg: fledgling
that leaves the nest in birds). In many cases, the young
leave the home in the process known as natal dispersion.
But there are exceptions noted, particularly among birds,
in the case of "co-operative breeding". This is where
young from previous years aid the parents in raising 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 feed
themselves. The reason may include guiding the offspring
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 36
on the first migration.

Scott (1980) investigated PPC by Bewick's swans

(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 predictions
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 feeding

on foods that produce aggressive encounters (eg:
agricultural crops);

3. Cygnets of smaller body size and females will remain

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, each for
1 min every 10 min, such that A was watched for 1 min,

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 37
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" (p940).
During that sample minute, all aspects of the birds
interactions were recorded including distance to mate,
cygnet, or parents; and distance to three nearest
unrelated neighbours. Event sampling was used for
aggressive encounters (table 3.5).


Description Record what individual Record details of an event
is doing at point in every time it occurs
Advantage Record for all Records key event as often
individuals being as it happens
Disadvantage May miss information Tends to look at the event
because focused on one out of context of other
individual at a time behaviour

Table 3.5 - Point and event sampling in observations.

Cygnets were significantly more successful in

aggressive encounters when near parents (within 4 swan
lengths) than alone (75% vs 33% won; X² = 4.2; df = 1;
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 flocks).

2. When the flock was eating waste potatoes that produced

more aggression, the cygnets remained approximately half
as near to parents compared to feeding on winter wheat
where less aggression occurred. Mean relative distance of
cygnet to parent was 1.0 for wheat and 0.6 for potatoes

3. Females and smaller cygnets remained closer to


The cygnets were more confident closer to parents as

shown by amount of time feeding: over 80% for those in
close proximity compared to less than 40% when cygnet was
seven or more swan lengths away.
PPC meant that parents intervened in aggressive
encounters on behalf of their cygnets (34% of
encounters), and the presence of parents was enough in
some cases to step aggression developing, especially with
subordinate birds.
But intervention had a cost for the parents, if only
to stop them feeding. For example, during October-
November, parents spent under 60% of time feeding

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 38
compared to 80% for adult pairs without cygnets.
The proximity changed over the winter period,
however, and it was reduced by January-February (mean
relative distance of 1.27 vs 0.72 in November-December).
As the cygnets moved further away, the parents spent more
time feeding (80% of time in February-March). There were
other beneficial changes in parents' behaviour over the
winter (table 3.6).


Mean percentage of observations
when adults alert (ie: heads up
in vigilant position):
Oct-Nov 40 20 <0.05
Dec-March 20 25 ns
Threat frequency (per min)
during feeding:
Oct-Nov 2.4 1.2 <0.02
Dec-Feb 2.0 1.2 ns

Table 3.6 - Changes in two behaviours of parents over the


Any direct costs to parents, like reduced feeding,

while involved in PPC is compensated by "indirect
fitness" in the survival of the offspring through feeding
or protection from aggression by unrelated adults.
Table 3.7 summarises the main advantages and
disadvantages of PPC.

1. Indirect fitness with a 1. Cost to parents in terms of
greater chance of the offspring's less opportunity for feeding.
survival and their production of
offspring. 2. Cost to parents in terms of
less opportunity for mating and
2. To teach offspring key further offspring.
survival skills like food sources
and migration. 3. Risk to parents in protecting
3. To protect offspring from
predators and aggressive 4. Offspring may not be able to
conspecifics (feeding fend for themselves when PPC
competition). ends.

4. The offspring benefit in terms 5. Offspring that need PPC can be

of protection and feeding. highly vulnerable in the first
few days, weeks, and months.
5. PPC means that offspring can
still developed after

Table 3.7 - Main advantages and disadvantages of PPC.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 39

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 gestation
lengths (236.1 vs 234.2 days for females), significantly
heavier birth weight (6.72 vs 6.23kg), and suck from
their mothers significantly more frequently (5.1 vs 2.6
daily suckling bouts). Also hinds who reared male calves
were less likely to produce a calf the following breeding
season, and those that did, gave birth later in the
season compared to mothers of female calves (Clutton-
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 animals
which the subject threatened or displaced to animals
which threatened or displaced it weighted by the identity
of the animals displaced" (Clutton-Brock and Godfray
1991) (table 3.8).



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 conditions
produce daughters. This is known as the Trivers-Willard
hypothesis (Trivers and Willard 1973).
The maternal conditions will be linked to the
resources available to survive and raise the offspring.
Where resources are plentiful, then the maximum genes can
be passed into future generations by male offspring based
on grandchildren (figure 3.2). Daughters will always find
a mate even if this limits the number of grandchildren.
The production of daughters is a better strategy where
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 40
resources are limited.


↓ ↓


↓ ↓


↓ ↓ ↓ ↓


↓ ↓ ↓





Figure 3.2 - Different strategies for offspring in

different maternal conditions.

The dominance of the female will also influence the

success of the offspring. High-ranking hinds produce more
sons because of the greater lifetime reproductive success
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-ranking
females produce more daughters. Increasing population
density is an example of poor maternal conditions, and
thus the production of daughters is a better evolutionary
However, Cockburn (1999) argues that male foetuses
are more sensitive to resource availability, and more of
them may be dying before birth with the increasing
population density. The increase in female births is in
fact the increased survival of females at birth.

It is unclear how the process of "choosing" the sex

of the offspring works. For example, the hormones from
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 (Cartwright
2000). Maybe high-ranking hinds have more testosterone as
well, and this explains the situation in red deer.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 41
Breder, C & Rosen, D (1966) Modes of Reproduction in Fishes New York:
Natural History Press

Cartwright, J (2000) Evolution and Human Behaviour Basingstoke:


Clutton-Brock, T.H & Godfray, C (1991) Parental investment. In Krebs,

J.R & Davies, N.B (eds) Behavioural Ecology: An Evolutionary Approach (3rd
ed) Oxford: Blackwell Science

Clutton-Brock, T.H et al (1981) Parental investment in male and female

offspring in polygynous mammals Nature 289, 487-489

Clutton-Brock, T.H et al (1986) Great expectations: Dominance,

breeding success and offspring sex ratios in red deer Animal Behaviour 34,

Cockburn, A (1999) Deer destiny determined by density Nature 399,


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 prolonged parental care in

Bewick's swans Animal Behaviour 28, 938-952

Trivers, R (1972) Parent-offspring conflict American Zoologist 14,


Trivers, R & Willard, D (1973) Natural selection of parental ability

to vary the sex ratio of offspring Science 179, 90-92

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 42
4.1. Introduction
4.2. Examples of lek behaviour
4.3. References


Lek polygyny is a specific type of polygamy where

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 before
mating with the best male. Good quality males get to mate
with many females, and females can mate only with the
best male (table 4.1). Parental care is solely the
concern of females in such species.

1. Convenient for females to 1. The system is open to
assess all the males in one place exploitation by poor quality
and choose the best quality. males who lurk near the best
quality males and attempt
2. Works well in normally forcible copulation.
geographically dispersed species
that come together at the 2. Best quality males may run out
breeding season only. of sperm for late-arriving
3. Good quality males get to mate
with many females. 3. Risk of interference from
males in neighbouring leks.
4. No costs to males of
maintaining territory for long 4. Problem of best quality males
periods of time. being temporarily monopolised by
other females.
5. Females can mate in lek
without being harassed by other 5. Females do not know if males
males. with leks near centre are "honest
signals" of good quality.

Table 4.1 - Main advantages and disadvantages of lekking.

When males establish their mating territory,

resources are generally not important as in a "normal"
territory which is defended because of its resources. 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).


Wikelski et al (1996) studied the marine iguanas

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 43
(Amblyrhynchus cristatus) on Genovesa island (Galápagos
archipelago, Ecuador). The mating season lasts from early
December to early January, and three seasons were
Individual animals were marked by hot branding which
left an identifiable mark while causing only superficial
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 along
the beach area. Focal (or point) observations were made
at four locations, and all copulations were recorded
(behaviour sampling) 6.
Three types of males were observed:

 Territorial males who occupied and defended a

particular mating area for five consecutive days. They
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 moved

around attempting to forcefully mate with any females
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 (table
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 "hotspot
phenomena" - small territorial males get "accidental
matings" when near large territorial males.


Body mass (g) 657 503 424
Total copulations 129 6 6
Copulations per male 3.1* 0.4 0.3

(* = significantly different to other two; p = 0.01)

(After Wikelski et al 1996)

Table 4.2 - Mating success of different types of male

iguanas in the 1992-3 breeding season.

Focal or point sampling records what is happening at a particular moment in time, while behaviour
sampling records every occasion of a particular behaviour.
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 44
A lek is like a "male beauty contest" for the
females. Comparison is possible to aid the choice of
males. What are the characteristics of males that improve
their mating success in this "beauty contest"? Many
studies have looked at individual species using "vote
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-analysis
(Hunter and Schnidt 1990) of forty-eight studies.
Table 4.3 summarises the characteristics analysed.


Attendance - time spent on lek Positive correlation: more time
Display frequency; eg: amount of Positive correlation: more time
time spent calling
Fighting frequency Positive correlation: more
Location of territory Negative correlation: nearer lek
Size of territory No correlation
Male body size Weak positive correlation: larger
Extravagant morphological traits; Positive correlation: larger
eg: antlers
Male age Positive correlation: older

Table 4.3 - Characteristics of males that gain mating

success in leks.

Meta-analysis (Glass 1977) allows the "quantitative

summary of statistical tests from multiple studies"
(Fiske et al 1998) by standardising the data (through the
effect size), and making general conclusions. However,
there are limitations to this technique (Fiske et al

i) Sample size of studies to use can be small; eg:

nine studies on fighting frequency, and seven on age.

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 results

tend to get published, so it is not known how many non-
significant studies were performed and not published.
Thus published studies may be unrepresentative of all the
studies performed. Statistical techniques have been
developed to overcome this problem (eg: number of studies
needed to change effect size; Rosenthal 1979).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 45
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 signals"

of the male's quality. The usual signals are body size
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 ability to
maintain such a territory if the signal is honest. The
signal will not be honest if there is "queue-jumping".
This is where fighting occurs, for example, and a lower-
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 in
central Finland over a eight-year period. The males at
the centres tended to be superior in terms of fighting
and survival abilities. Queue-jumping tended not to
happen often because of the risks of injury from fights.
The males queued for central lek territory (ie: waited
until high-ranking males leave). It is an "evolutionary
stable strategy" (Maynard Smith 1982) - the best strategy
in terms of costs and benefits.

(Source: Gagea; in public domain)

Figure 4.1 - Black grouse in Sweden.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 46
It is generally assumed that females will mate only
once with the best quality male, but this is not always
the case as with, for example, the ruff (Philomachus
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 the
lekking season. The other is lighter and hangs around the
mating courts ("satellite behaviour")(Lank et al 2002).
Lank et al (2002) studied the mating behaviour of
female ruffs (called "reeves") on a shoreline in Finland.
About a quarter were observed to mate with more than one
male on a single visit to the lek, and 17 of thirty-four
broods had multiple fathers. Fourteen out of 23 reeves
observed mated with both types of males.

Why do reeves mate with multiple males? The simple

answer is to diversify the genetics of the offspring. The
costs for females of multiple matings are low because
they do not risk the loss of paternal care as male
support does not occur. "For whatever reason, a female’s
mating rule in many lekking species may be not the oft-
stated search for the highest quality male, but rather to
seek several high quality mates" (Lank et al 2002 p214).

Beehler, B.M & Foster, M.S (1988) Hotspots, hotspots and female
preference in the organisation of lek mating strategies American Naturalist
131, 203-219

Fiske, P et al (1998) Mating success in lekking 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 polyandry in a lek mating

system Behavioural Ecology 13, 2, 209-215

Maynard Smith, J (1982) Evolution and the Theory 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 iguanas: Female grouping

and male reproductive strategies Animal Behaviour 52, 581-596

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 47
5.1. Post-conception mating
5.2. Homosexual interactions
5.3. References


Sex is about reproduction among animals. Yet non-

reproductive sex exists, for example, by pregnant or
lactating females. What are the reasons for such
behaviour, particularly among females (also known as
post-conception mating)? Table 5.1 lists the advantages
and disadvantages for males and females.

MALES 1. Pleasure. 1. Waste of sperm and cost of
replenishing supply.
2. Strengthens the bond
in monogamous species. 2. Energy costs of sex.

3. Male sexual 3. Risks of sexually

competition. transmitted disease.
FEMALES 1. To gain favour with 1. Risks of injury during sex.
dominant males.
2. Risks of sexually
2. To gain protection for transmitted disease.
self and offspring from
dominant males. 3. Does not confuse male about
paternity if he knows that sex
3. To confuse males about non-reproductive (eg: female
paternity and gain shows signs of pregnancy).
support, and/or avoid
infanticide. 4. Energy costs of sex.

4. Female sexual
competition by reducing
sperm of male available
to other females.

5. Pleasure.

6. Strengthens the bond

in monogamous species.

Table 5.1 - Advantages and disadvantages of non-

reproductive sex.

Stoinski et al (2009) observed one male gorilla with

four females at the Zoo Atlanta in the USA. The group of
five western lowland gorillas (Gorilla gorilla
gorilla)(figure 5.1) were observed for a total of 273

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 48
hours over 245 days between December 2004 and December
2006. Females encouraging sex (solicitation) was defined
as "slowly approaching male with direct eye contact,
often accompanied by pursued lips and attempts to touch
the male" (p588).

(Source: Arpingstone; in public domain)

Figure 5.1 - Male gorilla.

Non-reproductive females offered sex when other

females were sexually active (table 5.2).


Single 36 17 6 3 10
occurrence days
- only one
female sexually
Co-occurrence 75 20 9 17 29
days - another
female sexually
Significance <0.05 ns <0.05 <0.01 <0.01

(After Stoinski et al 2009)

Table 5.2 - Solicitations by four female gorillas.
Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009
ISBN: 978-1-904542-47-6 49
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 females by
depleting his sperm.
When there is more than one male, non-reproductive
sex by the female is a way of confusing the male about
paternity, and thereby encouraging him to care for her
and her offspring.


A different aspect to non-reproductive sex is where

same-sex individuals court and attempt to mate -
"homosexual interactions" (Maklakov and Bonduriansky
2009). Such behaviour may assert dominance over rivals,
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 than
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 energy
loss through the "dance" and injury during fights;

 Seed beetle (Callosobruchus maculatus) - Males chase

females and mount without courtship. Sex is dangerous
for females as the penis has spines attached. The cost
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 measured in

terms of deaths in six experimental conditions - males
and females alone, all male and all female groups, and
males and females in mixed sex groups. In both species,
males in all male groups had shorter lifespans.
In terms of evolution, male homosexual mounting in
insects is the product of the benefits of rapid,
indiscriminate mating over the costs of discriminating
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.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

ISBN: 978-1-904542-47-6 50
Aiken, R.B (1981) The relationship between body-weight and homosexual
mounting in Palmacorixa nana Walley (Heteroptera: Corixidae) Florida
Entomologist 64, 267-271

Maklakov, A.M & Bonduriansky, R (2009) Sex differences 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 sexual competition American
Journal of Primatology 71, 7, 587-593

Thornhill, R & Alcock, J (1983) The Evolution of Insect Mating Systems

Cambridge, MA: Harvard University Press

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009

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