Burns Et Al. 2011. Male Reproductive Traits and Their Relationship to Reproductive Traits in Their

8/11/2019 Burns Et Al. 2011. Male Reproductive Traits and Their Relationship to Reproductive Traits in Their

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Review Article

Male Reproductive Traits and Their Relationship to Reproductive Traits in Their

Female Progeny: A Systematic Review

BM Burns1, C Gazzola2, RG Holroyd2, J Crisp3 and MR McGowan3

1The University of Queensland, Centre for Animal Science, Queensland Alliance for Agriculture and Food Innovation, Rockhampton, Qld, Australia;2Department of Employment, Economic Development and Innovation, Rockhampton, Qld, Australia; 3The University of Queensland, School ofVeterinary Science, Gatton, Qld, Australia

Contents

The overall objective of one of the major research programs inthe Co-operative Research Centre (CRC) for Beef GeneticTechnologies is to Improve female reproductive performance

in tropical, northern Australian beef cattle herds. To addressthis overall objective, a quantitative genetics project focusedon investigation of male reproductive traits was designed andlinked to three female reproductionfocussed projects, (i)discovery of genes associated with post-partum re-conceptionand age at puberty; (ii) expression of genes associated withpost-partum re-conception; and (iii) early predictors of lifetimefemale reproductive performance. During the initial planningof this male reproductive traits project, the CRC ScientificReview Committee recommended that the research teaminvestigate and evaluate potentially new, early-life (i.e ableto be measured before 2 years of age) predictors of both maleand female reproductive performance. To address this recom-mendation, the following was carried out: (i) criteria forselection of traditional and candidate traits were established;

(ii) methodology for tabulation of potential traitsphenotypesthat define male and female reproductive function wasdeveloped; and (iii) a systematic scientific review of early-lifepredictors of male and female fertility was prepared. Thisreview concluded that although factors that might be useful inpredicting male reproductive performance have been studiedfor many years, there was relatively little useful informationavailable to meet the objectives of this review. It was alsoconcluded that the direction of future research should beguided not only by previous research which was scarce, butalso by speculative hypotheses arising from an understandingof the physiological, endocrinological and genetic processesactive in reproduction. A small number of new traits wererecommended in addition to traditional sperm morphology,sexual behaviour, anatomical structure and growth traits.

Potential additional traits include measurement of gonadotro-phin-releasing hormone-stimulated luteinizing hormone(GnRH-stimulated LH); inhibin; several seminal plasma pro-teins (osteopontin, spermadhesin and seminal plasma proteinsBSP30 and phospholipase A2 could be used in an index); 11b-hydroxysteriod dehydrogenase; and leptin. In addition, thepotential also exists to screen animals for a number of geneticmarkers associated with age of puberty, follicular recruitmentand ovulation rate and genes associated with bovine seminalplasma protein and testosterone production. Insulin-likegrowth factor-1 (IGF-1) measurements are included becauseof their association with growth parameters, and an additionalanalysis demonstrated associations with male and femalereproductive traits. Some of these factors have been previouslyevaluated in small numbers of animals of various species under

intensive management conditions. Therefore, there is a need toevaluate these factors in much larger numbers of beef cattlegrazing semi-extensive tropical production systems in northern

Australia to determine their value in improving beef cattleenterprise profitability through improved herd fertility.

IntroductionA major limitation to northern Australian beef cattleherds is that direct selection for cow fertility can onlybe applied to females, usually at low intensities, andrelatively late in life when the cows have one or twocalving records (Mackinnon et al. 1989). This problemcould be overcome if herd traits in males wereidentified that were genetically correlated to femalefertility traits, and these male traits were able to bemeasured early in life (Mackinnon et al. 1989). Inaddition, Walkley and Smith (1980) reported in sheepthat if a trait could be identified in young males,which was correlated with the reproductive perfor-mance of adult females, the potential would exist todouble the selection intensity, and therefore the rate ofgenetic change, by selecting in both males andfemales.

Land (1973) proposed that because the hormonalcontrol of reproductive function is similar in the twosexes, one might expect that male and female reproduc-tive traits would be closely correlated genetically.Darwash et al. (1999) have also reported that there isa growing body of evidence suggesting that the majorityof endocrine factors associated with reproduction indairy cattle are a result of differential gene expression inthe hypothalamus, pituitary, ovary and uterus.

In conclusion, it may be possible to identify early-life

predictors of fertility both phenotypically (a bullsfertility as reflected by improved calf output) andgenetically (the fertility of a bulls female and maleprogeny). To further investigate the potential use of thisapproach to improve the reproductive performance ofbeef cattle, in particular tropically adapted genotypes, asystematic review of the published literature on malereproductive traits and their relationship to reproductivetraits in their female progeny was conducted.

Objective of the Review

To identify male traits potentially genetically correlatedwith female fertility traits, with particular emphasis on

identifying traits which could be assessed in pre-pubertalbulls.

Reprod Dom Anim 46, 534553 (2011); doi: 10.1111/j.1439-0531.2011.01748.x

ISSN 0936-6768

The State of Queensland (through the Department of Employment, Economic Development and Innovation) 2011


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Materials and Methods

The systematic review was conducted as follows:

1. Publications were reviewed to examine the rela-tionship between various bovine male traits and thefertility of the male andor the fertility of his male or

female offspring. Non-bovine mammalian publica-tions were also examined.2. The search was restricted to testicular, seminal andhormonal traits only as mating behaviour can only bemeasured reliably in sexually mature bulls.3. Those publications that quantified the relationshipbetween measured traits and fertility and providedestimates of the heritability of traits and the geneticcorrelations between male and female traits wereexamined in detail.4. Traits that, from a developmental (embryological)or physiological (endocrinological) point of view,have the potential to predict both male and female

reproductive function were considered.The selection criteria for candidate early-life predic-

tors of male fertility and fertility of male and femaleoffspring were as follows:

1. Male traits that were moderately heritable andmoderately genetically correlated with female traitswere given an initial high ranking.2. Consideration was given to potential novel traitswhose case for selection could be based on thetheoretical potential of the trait to predict fertilitybased on whatever direct or derived knowledge wasavailable.3. Traits were grouped according to those that could

be measured in the pre-pubertal bull and those thatcould only be measured after the bull reachedpuberty. Within each of these categories, traits werefurther grouped according to their capacity to assessone of the followings:

(i) Testicular development;(ii) Endocrine control of testis function;(iii) Spermatogenesis; and(iv) Fertilizing potential of sperm.

4. Traits that require sampling methods that arehighly invasive, require multiple samples to becollected and are very expensive or detrimental tothe future fertility of the animal were given an initiallow ranking.

Results and Discussion

The findings from this systematic review have beensummarized to four tables (Tables 14) under thefollowing headings:

1. Male reproductive traits and their relationship toother measures of reproductive function in the male.2. Male phenotypic traits and their correlated traits infemale progeny.3. Heritability of male traits and correlated femaleprogeny traits.

4. Genetic markers of male reproductive traits witheffects on female progeny.

Age-corrected scrotal circumference was consistentlyreported to be a useful method of assessing reproductivefunction in bulls (Table 1) because of the favourablerelationship with a number of sperm traits (Brinks et al.1978) and fertility (Mackinnon et al. 1990b). Pre-pubertal basal serum follicle-stimulating hormone

(FSH) concentration was identified as a potentialcandidate trait because of its role in the endocrinecontrol of testicular function and its moderate correla-tion with Sertoli cell number (Moura and Erickson1997) (Table 1). The reported moderate correlationbetween pre-pubertal basal serum luteinizing hormone(LH) concentration and age of puberty also suggestedthat this trait may be a useful early-life predictor offertility (Aravindakshan et al. 2000) (Table 1). How-ever, these measurements require multiple samplingunder commercial industry conditions.

In contrast, GnRH-stimulated release of LH in pre-pubertal bulls reported by Moura and Erickson (1997)

and Bagu et al. (2006) may be a practical alternative(Table 1). This test is simpler than multiple samplings asit requires an initial pre-injection blood sample, followedby an injection of GnRH analogue, and a subsequentsingle 0.5 to 1 hourly blood sample. However, there areonly a small number of publications describing the useof this test, and except for one study in bulls from1626 months of age (Perry et al. 1990a), most studieshave only monitored the bulls to yearling age (Mouraand Erickson 1997; Bagu et al. 2006) (Table 1). Perryet al. (1990a) reported that the best fertility indices,which included GnRH-stimulated LH, were thoseassessed at 11, 8, 6 and 2 months prior to mating andwere collectively significantly correlated with pregnancy

rate (P < 0.01). However, Perry et al. (1990a) alsoreported that these tests carried out on the bullsimmediately prior to and immediately post-mating didnot result in strong correlations with pregnancy rates. Inaddition, in two separate studies using four Hereford-Shorthorn bulls and three Zebu British cross-bredbulls (bulls aged 1729 months were individually joinedwith groups of 1930 cows), respectively, Post et al.(1987) reported that the bulls with the highest peakplasma testosterone concentrations 22.5 h after intra-muscular injection with GnRH achieved the highestoverall fertility [capable cows pregnant; highest libido(oestrous cows mated) and fertilizing ability (mounted

cows pregnant)]. Further, the rankings of the Bos indicusbulls for both reproductive performance and testoster-one response to GnRH were repeatable when measuredat two and four years of age (Post et al. 1987).Therefore, these studies suggest that it would be usefulto conduct a study of GnRH-stimulated release of LH inpre-pubertal bulls at around 23 months of age and thenevaluate these animals through puberty up to 2 years ofage. The GnRH-stimulated LH relationship with testesfunction, in terms of age at puberty and age at which anormal spermiogram is recorded, could be investigatedgiven the experimental design of the CRC Maleindicator traits to improve female reproductive perfor-mance Project. However, it is acknowledged that

conducting the GnRH response test is reasonably labourintensive.

Male and Female Reproductive Traits 535



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Table1.Malereproductivetraitsandtheirrelation

shipwithothermeasuresofreproductivefunctioninthemale(a)Pre-pubertaltraits;(b)post-pubertaltraits(>2yearsold)

MaleTra

it

Reference

SpeciesBreed

Age

SampleType

MaleCorrelatedTraits

rg

rp

Comments

(a)Pre-p

ubertaltraits

CorrectedSC

(SCA

ge)

Brinksetal.(1978)

Cattle;H,A

12mo

l

Motility%

%

primaryabnormality

%

secondaryabnormality

%

normal

0.25

)0.51

)0.42

0.58

Sc

rotalcircumference

fa

vourablycorrelated

w

ithallsementraits

evaluated.

n=

287

Mackinnonetal.(1990

b)

Cattle;Dr

9mo

12mo

18mo

l

DifferenceinSCbetweenhigh-

and

low-fertilitylines(EBVforP

R)

HighLow5.8mm

HighLow9.6mm

HighLow16.0mm

n=

111

Follicle-s

timulating

hormon

e(basalFSH)

MouraandErickson(19

97)

Cattle;A

212mo

23mo

812mo

912mo

sm

YearlingSC

Sertolicellnumber

RS

)0.53to)0.74

)0.51to)0.54

)0.47to)0.53

)0.56to)0.64

n=

24

RS(roundspermatids

perSertolicell)

Aravindakshanetal.(20

00)

Cattle;HC

110mo

sm

Agepuberty

ns

n=

20

Basedon2smallgroups

selectedforagepuberty

Luteinizinghormone

(meanL

H)

MouraandErickson(19

97)

Cattle;A

212mo

sm

YearlingSC

ns

n=

24


00)

Cattle;HC

1mo

2.5mo

9mo

sm

Agepuberty

)0.56

)0.51

)0.76

n=

20

Basedon2smallgroups


Luteinizinghormone

(pulsefrequencyLH)


00)

Cattle;HC

2.5mo

5mo

sm

Agepuberty

)0.67

)0.51

n=

20

Basedon2smallgroups


Testoster

one

MouraandErickson(19

97)

Cattle;A

212mo

sm

YearlingSC

ns

n=

24


00)

Cattle;HC

110mo

sm

Agepuberty

ns

n=

20

Basedon2smallgroups


Gonadotrophin-releasing

hormon

estimulatedFSH

(GnRH-stimulatedFSH)

MouraandErickson(19

97)

Cattle;A

212mo

sm

YearlingSC

nsto)0.71

n=

24

Cou

ldbeusefulatsome

age

s,butdatanotgiven


00)

Cattle;HC

110mo

sm

Agepuberty

ns

n=

20

Basedon2smallgroups


GnRH-stimulated

testosterone

MouraandErickson(19

97)

Cattle;A

3mo

212mo

sm

YearlingSC

Testosterone

0.48

0.48to0.56

n=

24

GnRH-stimulatedLH

Haleyetal.(1989)

Sheep

2.55mo

sm

Selectionlines

GnRH-stimFSH

SCatsameage

0.400.14

Perryetal.(1990a)

Cattle

16mo

18mo

20mo

24mo

26mo

sm

PR

0.710.760.730.660.45

Severalbreeds,goodif

holdsuppre-puberty.

Inconvenient

me

asurementprocedure

MouraandErickson

(1997)

Cattle;A

212mo

sm

BasalLH

BasalFSH

GnRHstimFSHa

GnRHstimFSHb

0.650.480.690.75

aandbDifferenttimes

afterstimulation

536 BM Burns, C Gazzola, RG Holroyd, J Crisp and MR McGowan



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Table1.(Continued)

MaleTra

it

Reference

S

peciesBreed

Age

SampleType

MaleCorrelatedTraits

rg

rp

Comments

Aravindakshanetal.

(2000)

Cattle;HC

110mo

sm

Agepuberty

ns

n=

20

Bas

edon2smallgroups

selectedforage

puberty.

Somestatisticsof

concernwith

sub-groups

Baguetal.(2006)

Cattle,HC

15mo

sm

Predictearlypuberty

(significantp

Documents

Burns Et Al. 2011. Male Reproductive Traits and Their Relationship to Reproductive Traits in Their