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J Theor Biol 2014 Grafen A

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© All Rights Reserved

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journal homepage: www.elsevier.com/locate/yjtbi

Total reproductive values for females and for males in sexual diploids

are not equal

Alan Grafen a,b,n

a

b

Zoology Department, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom

A U T H O R - H I G H L I G H T S

I perform an age- and sex-structured population calculation of reproductive value.

Fisher's result is recovered with the additional assumption of demographic stability.

Total reproductive value of a sex is proportional to its average age at parentage.

Total reproductive values of female and male offspring are equal.

art ic l e i nf o

a b s t r a c t

Article history:

Received 10 February 2014

Received in revised form

1 May 2014

Accepted 12 May 2014

Available online 21 May 2014

A very simple mathematical exposition of reproductive value in an age- and sex-structured sexual

diploid population employs reproductive value as the probability that a random gene in a distant

generation traces its ancestry to a given individual or set of individuals today. Although the total

reproductive values of all females and that of all males are not in general equal, but instead proportional

to the average age of a new mother and a new father, respectively, Fisher's equal-investment conclusion

for the sex ratio remains valid because the total reproductive value of age-zero females equals the total

reproductive value of age-zero males. However, the conclusion is seen to require an extra assumption,

namely stability of the age-distribution.

& 2014 Elsevier Ltd. All rights reserved.

Keywords:

Sex ratio

Equal investment

Diploidy

Overlapping generations

Structured populations

1. Introduction

Fisher (1930) introduced the concept of reproductive value, and

made two quite different applications of it, both with far-reaching

effects. Dividing the population into age classes, he attributed a

reproductive value to individuals of different ages, and this

quantity is central in modern demography. The central point of

the argument in the second application begins by considering how

parents invest in offspring, and continues

Let us consider the reproductive value of these offspring at the

moment when this parental expenditure on their behalf has

just ceased. If we consider the aggregate of an entire generation

of such offspring it is clear that the total reproductive value of

n

Correspondence address: St. John's College, Oxford OX1 3JP, United Kingdom.

Tel.: 44 1865 277438.

E-mail address: alan.grafen@sjc.ox.ac.uk

http://dx.doi.org/10.1016/j.jtbi.2014.05.021

0022-5193/& 2014 Elsevier Ltd. All rights reserved.

the males in this group is exactly equal to the total value of all

the females, because each sex must supply half the ancestry of

all future generations of the species (Fisher, 1930, p. 142),

and Fisher goes on to draw the basic sex ratio result that equal

investment is the outcome of evolution under assumptions including panmixia and diploidy. With discrete, non-overlapping generations, it does indeed follow that the female offspring and male

offspring must have exactly equal contributions to future generations, but with overlapping generations, it is even possible, for

example, that this particular generation of males never mates, and

the females mate with older males. Formal treatments of this

argument (e.g. Shaw and Mohler, 1953; Bodmer and Edwards,

1960) usually assume discrete non-overlapping generations. Fisher's argument therefore seems to depend on non-overlapping

generations, but is frequently applied in other situations (West,

2009). The current paper calculates reproductive values for a

population divided simultaneously by age and sex, works out the

234

versus all males and female offspring versus male offspring, and

then considers the robustness of the equal investment result.

We consider a diploid dioecious population in discrete time

with overlapping generations. We assume that the population is

sufciently mixing that it makes sense to select a random gene in

some very distant generation, and dene the probability that its

unique ancestral path passes at time t to an offspring (a 0) from

an individual of a given age, a A f1; 2; 3g and sex s A ff ; mg, say

utsa. We consider the paths to pass just after time t, so that at time

t itself the path is with the donor not the recipient of the gene.

Autosomal genes are studied, so whenever a gene's ancestral path

jumps from one individual to a parent, there are equal chances

that the parent is female and male, and we assume that the

probability distributions of the ages of the new parents at time t

are ptfa and ptma (so a ptsa 1). We assume that the gene and its

alleles are selectively neutral. A path that jumps from a parent of

age a to an offspring must be present in the parent all the way

back to age zero, when it passes to one of the parent's own

parents. Let the chance that an ancestral path moves between

individuals at time t be ht, so the chance that it remains within the

same individual is 1 ht . We can write this as

utsa

ht

p :

2 tsa

an individual of a given age a and sex s, vtsa, comprises two

mutually exclusive possibilities, that the ancestral path passes to a

descendant in this period, and that the path is present at time t 1

in an individual of age a 1. An ancestral path is always somewhere at each time, so s;a vtsa 1. The probabilities of mutually

exclusive events add, so

1

i0

1

vts0 ut i;s;i :

i0

quantities varies with time, and we accordingly omit the t-subscript.

The above equations now imply

1

vf 0 ufi

i0

1

h 1

h h 1

p p u vm0 :

2 i 0 fi 2 2 i 0 mi i 0 mi

equals the total reproductive value of all age-zero males. We note

that each equals h/2, which makes sense as we are dening

reproductive value as the probability that a random distant gene

traces back to the newborns today. The result is a natural one. The

probability that an ancestral path intersects newborn females

today equals the probability that it jumped into a one-year old

female in one year's time, plus the probability that it jumped into a

two-year old female in two years time, and so on. Now under

stable demography, these probabilities do not depend on the time

at which the jump occurs, and so we may align them all in the

same year, converting a diagonal sum across years into a vertical

sum, which equals the chance that the path jumps into a female of

any age this year. But these vertical sums must be equal for males

and females, for next year's newborns have one father and one

mother, and a gene goes equally likely to one and the other.

1

a

a i0

value of all females to the reproductive value of age-zero females

equals the average age of a new mother, and mutatis mutandis for

males; and so the ratio of the total reproductive value of all

females to that of all males equals the average age of a new mother

divided by the average age of a new father. This result has a simple

interpretation. As we trace back the ancestral path of a given allele,

it leaps backwards into female and male bodies, and with equal

probability at each leap. Its average sojourn time in a female body

is the average age of a new mother, and in a male body is the

average age of a new father. Hence the chance of nding it at any

one point in time in a given sex is proportional to the average age

at which the path enters that sex.

Note that the sum of the total reproductive value of females

and of males equals one, as the ancestral path of a future allele

rests in exactly one individual at any given time t. Hence the total

reproductive value of all females equals the average age of a new

mother divided by the sum of the average ages of a new mother

and a new father.

3. Discussion

The total reproductive value of all females and of all males is

not in general equal in dioecious diploids in discrete time with

overlapping generations, casting doubt on a crucial step in Fisher's

sex ratio argument. In view of the empirical success of sex ratio

theory (West, 2009), it is fortunate that his equal investment

conclusion survives a more general analysis. However, it was

necessary to make the assumption of demographic stability to

achieve this result. The total reproductive values of age-zero

females and males are indeed equal in this case, and Fisher's

argument can therefore proceed unhindered from the passage

quoted above to the famous conclusion of equal investment. The

total reproductive values of all females and of all males are shown

very naturally to depend on how old an average new mother and

average new father are.

Sex ratio is a major topic in behavioural ecology today, and the

standard reference is West (2009). Following Hamilton (1967),

many exceptions to Fisher's conclusion are now conceptually wellunderstood and empirically well-documented as not meeting his

assumptions, and sex ratio has the best quantitative match

between theory and data in modern adaptationist biology. One

relevant nding here is that unequal reproductive values of all

females and all males have been noted before, in the study of sex

ratio in Hymenoptera with overlapping generations, in the socalled sphecid and halictid patterns of partial bivoltinism (Seger,

1983; Grafen, 1986), which are simple examples where demographic stability does not hold for every single generation (though

it could be reasonable to assume that it held for pairs of generations so that all even generations were the same as each other, and

all odd generations were the same as each other). However, those

are haplodiploid models, and the phenomenon has not to my

knowledge been noted in diploid models before. Whereas nonoverlapping generations ensure equal total reproductive value of

females and males in each generation, overlap of generations will

generically cause differences to arise between them.

This lacuna in Fisher's argument has not, so far as I know, been

noted before. Fortunately, as we have seen, the major implications

for sex ratio theory are unaffected by studying reproductive value

in a sex- and age-structured population under demographic stability.

But the need for this assumption raises questions. Does random

Does systematic (e.g. seasonal) uctuation in age distribution

affect it? How does any effect depend on an individual's information about the age distribution or the season? In the light of the

answers to those theoretical questions, how reasonable is the

assumption of constant demography in empirical applications?

Acknowledgments

The author thanks Katja Lehmann and Andy Gardner for

comments, and declares no conict of interest.

235

References

Bodmer, W., Edwards, A., 1960. Natural selection and the sex ratio. Ann. Hum.

Genetics 24, 239244.

Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford University

Press, Oxford, UK (see Fisher (1999) for a version in print).

Fisher R.A.,1999. In: J.H. Bennett (Ed.), The Genetical Theory of Natural Selection,

Oxford University Press, Oxford, UK (Variorum Edition of 1930 OUP edition and

1958 Dover edition).

Grafen, A., 1986. Split sex ratios and the evolutionary origins of eusociality. J. Theor.

Biol. 122, 95121.

Hamilton, W.D., 1967. Extraordinary sex ratios. Science 156, 477488.

Seger, J., 1983. Partial bivoltinism may cause alternating sex-ratio biases that favour

eusociality. Nature 301, 5962.

Shaw, R.F., Mohler, J., 1953. The selective signicance of the sex ratio. Am. Nat. 87,

337342.

West, S.A., 2009. Sex Allocation. Princeton University Press, Princeton, New Jersey.

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