Variation of sperm length and heteromorphism in drosophilid species

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Variation of sperm length and heteromorphism in

drosophilid species

D. Joly, M.-L. Cariou, D. Lachaise, J.R. David

To cite this version:

Original

article

Variation

of

_sperm

_length

and

_{heteromorphism}

in

_drosophilid

_species

D.

_Joly

M.-L.

Cariou

D.

Lachaise

J.R. David

Centre National de la Recherche

_Scientifi

_q

_ue,

laboratoire de

_biologie

et

_{genetique evolutives,}

91198

_{Gif-sur- Yvette Cedex,}

France

(received

8 December

1988, accepted

17

_April

₁₉₈₉₎

Summary -

Sperm length

was measured in 27

drosophilid species,

and a

_general

survey

of size variation is

_presented

for 75

_species

for which information is available. Mean

length

varies from 0.113 mm in the D. obscura group to almost 20 mm in the

_recently

investigated

D.

_littoralis;

in the latter case, sperm

length

is

nearly

6 times the male

body

length.

The

_{huge interspecific variability}

may be estimated

by

considering

the coefficient

of variation

_(c.v.)

between

_{species belonging}

to the same taxon. In _{the genus}

_Drosophila

the c.v. amounts to 130%

_{(64 species).}

The _average c.v. decreases in lower taxa,

being

for

_example

96% in

_subgenera

and 61% in

_species

_groups. More

_closely

related

_species

are thus less

_divergent,

but in any case sperm

length

must be considered as a fast

evolving trait, increasing

or

_decreasing.

Individual measurements of sperm

length

within a

species generally provide

a

_{unimonal, relatively gaussian}

distribution

(monomorphism).

By

contrast, 13

_investigated

species

of the D. obscura _group exhibited bimodal distributions. This

heteromorphism

may be considered as a stable

evolutionary

strategy in the D. obscura

group.

Drosophila - sperm length - sperm heteromorphism - sperm evolution

Résumé - Variation de la _longueur des _{spermatozoïdes} et hétéromorphisme chez les drosophilidés. La

_longueur

des

_{spermatozoïdes}

mesurés chez 27

_espèces

de

_{Drosophilidés}

est étudiée au niveau de l’ensemble de la

_famille

_{(75 espèces).}

Les moyennes de

longueur

varient de 0,113 mm chez les

espèces

du groupes obscura

jusqu’à

20 mm chez une

_espèce

nouvellement

_étudiée,

D.

littoralis;

chez cette

_dernière,

la

_longueur

du

_{spermatozoïde}

at-teint 6

_fois

la

_longueur

du _corps de l’adulte.

_{L’amplitude}

de la variation

_{interspécifaque}

peut être

_appréciée

en considérant le

_coefficient

de variation

_(c.v.)

entre

_espèces

appar-tenant à un même taxon. Dans le genre

Drosophila

(64

espèces

étudiées),

la valeur du

c.v. atteint 130%. Les valeurs des c.v. _moyens diminuent _pour les niveaux

_taxonomiques

inférieurs,

c’est-à-dire 96% au niveau du sous-genre et 61 % pour les groupes

d’espèces.

Les

_longueurs

de

_{spermatozoïdes}

des

_espèces

étroitement

_apparentées

sont relativement

proches

mais dans

quelques

cas, il

apparaît

que ce caractère évolue

rapidement, tendant,

soit à _augmenter, soit à diminuer. Les mesures de la

_longueur

des

_{spermatozoïdes}

pour

une

_{espèce correspondent généralement}

_pour un individu à une distribution

unimodale,

gaussienne

(monomorphisme).

En

_revanche,

les 13

_espèces

du groupe obscura montrent

des distributions bimodales. Cet

_{hétéromorphisme}

peut être considéré comme une

_stratégie

évolutive stable.

Drosophile - longueur des _{spermatozoïdes - hétéromorphisme} des spermatozoïdes

INTRODUCTION

In most

_Eucaryote

_species,

meiotic

_reproduction

has evolved in

_producing

two sizes of

_gametes,

known as the macro, or female

_gamete

_(oocyte

or

_ovum)

and

the

_micro,

or male

_gamete

_(sperm)

_respectively

_(Parker

et

_{al., 1972; Power,}

1976;

Maynard Smith,

1978;

Alexander &

_Borgia,

1979;

Parker,

1984).

In the

macrogamete,

size variations between taxa are well documented and

_incorporated

in the

_evolutionary

theories of

_parental

investment

_(Trivers,

₁₉₇₂₎

and life

_history

strategies

(Throckmorton, 1966).

By

comparison,

evolutionary

trends in the

_microgamete

_(sperm)

have

re-mained

_{neglected. Indeed,}

when

_considering

vertebrates an overall

_uniformity

seems the

_rule,

_yet

some differences in _sperm heads or tails have been found in

rabbits and rodents

_(Friend,

_1936;

_Beatty

&

_Napier,

_1960;

_Beatty

&

_Sharma,

1960;

Woolley,

1971).

In

_these,

_sperm with a medium size

_flagellum

less than 0.1 mm

_long

are

_produced

in

_huge

numbers and each

_gamete

has an

_extremely

low

_probability

of

_producing

a

_zygote.

_{Sperm shape,}

size and ultrastructure _are,

however,

far more diverse _among invertebrates

_{(Fain-Maurel,}

_1966;

Afzelius et

_al.,

1976; Baccetti, 1979;

Sivinski,

1984;

Chauvin et

_al.,

₁₉₈₈₎

and

_analysing

this

diver-sity

should

_help

to understand the

_{developmental}

constraints and selective pressures

which

permitted

or

_promoted

the various

_patterns

_presently

observed. In some

in-vertebrates,

including

Lepidoptera,

two or more

_{morphologically}

and

_functionally

different

_microgametes

occur

_{intraspecifically}

and warrant

_recognition

of _eusperm and parasperm

(Healy

&

Jamieson, 1981; Jamieson,

1987a).

In the

_present

_work,

attention is focused on the evolution of

_{sperm length}

in a

monophyletic

dipteran

taxon,

the

_family

_{Drosophilidae.}

_{Drosophila melanogaster,}

generally

considered as a reference for _{this group, is known for its}

_long

_sperm

(1.9 mm)

which is almost as

_long

as the

_body

of the

_fly

(Cooper,

_1950;

Yanders

&

_{Perras, 1960;}

_Beatty

&

_Burgoyne,

_1971;

Gould-Somerot et

_al.,

_1974;

_Joly,

1987).

However,

at the

_family

_level,

D.

_melanogaster

_sperm can _{appear very} short

compared

to those of other

_species

such as for instance D.

_hydei,

where it can be 4-5 times

_(1.4

or even 1.9

_cm)

the size of the

_body

of the

_fly

_(Hess

&

_Meyer,

_1963;

Jamieson,

1987b).

Taxonomists have

_long

been aware

that,

in the

_family

_{Drosophilidae,}

_sperm

length

could be _very variable between

_species

and several _papers have been

_recently

devoted to this

_problem

_(Beatty

&

_Sidhu,

1970;

Sanger

&

_{Miller, 1973;}

Gromko et

al., 1984;

Sivinski,

1984;

Hatsumi &

_Wakahama,

_1986;

Hihara &

_Kurokawa,

_1987;

Joly,

1987).

Explaining

such variations raises an

_{evolutionary challenge}

which _may

be formulated as follows: if _sperm

_length

is a fast

_evolving

_trait,

it should exhibit a

high

genetic

variance and a

_{high heritability,}

at least in some

_species;

_moreover, a

rapid

evolution for increased or decreased

_length

would be difficult to

_explain

if the trait is considered as

_neutral,

and

_strong

selective _pressures should exist or have existed

_during

the process of

speciation.

In

_{Drosophila, intraspecific}

_genetic

_variability

of _sperm

_length

is

_poorly

docu-mented and

_presently

available

_{investigations}

have failed to demonstrate

_genetic

variance

_{(Joly, 1987)}

or have found

_only

_{very limited}

_variability

_(Beatty

&

_Sidhu,

In the _genus

_Drosophila,

_sperm

_length

can indeed be considered as a fast

_evolving

trait with a loose

_relationship

with

_phylogeny.

In most

_species,

sperm

length

distri-butions

within

the individual are unimodal with a limited

variability. However,

in one

_monophyletic

_taxon,

the D. occurs

_species

_{group, the} occurrence of bimodal

distributions seems the rule and we therefore _argue here that it

corresponds

to an

evolutionary

stable

_strategy

_{(ESS) (Maynard}

_Smith,

_1974).

MATERIAL AND METHODS

Sperm length

was measured in 27

species,

13 of which

belong

to the obscura

species

group

including

the two

_recently

discovered East African

species

(D.

microlabis and

D.

_{kitumensis) (Cariou}

et

_al.,

_1988).

The source of material of the obscura group

species

investigated

was the same as in Cariou et al.

(1988)

with the

exception

of D.

_a

_f

_finis

_{(14012, 014-1)}

and D. azteca

_(14012-0171)

which were

_{provided by}

the

Bowling

Green Stock.

The

_eight

_species

of the

_{melanogaster subgroup}

were

_analyzed.

The source of

specimens

of the

_melanogaster

_{complex species}

was the same as in

Joly

(1987)

while those of the others were the

_following:

D. teissieri and D.

_yaku.ba

came from

different localities in Africa

_{(Gif Stock);}

D. erecta

_(Ivory

_Coast,

Gif

_220-5)

and

D. orena

_(West

_Cameroon,

Gif

_188-1).

Other

_drosophilid

_species

studied were D. bahunde

(Kenya,

Gif

269-4),

D.

bakundjo

(Kenya,

Gif

_269-5),

_{Scaptorrayza padlida}

_(Kenya,

Gif

_292-2),

Zaprionus

tuberculatns

_{(West-Africa),}

D.

_grimshawi

_(Hawaii)

and D. littoralis

_(unknown

Palearctic

_origin)

from the

_Bowling

Green Stock.

The strains were reared at 21 °C.

_Sperm

were recovered from the seminal vesicles of one or several males. The testes were isolated and

_opened

in a

_drop

of saline solution and the sperm allowed to

_spread

out. This

preparation

was observed under a

_microscope

with

_phase

contrast

_optics.

When _{the sperm} had ceased to _move,

_they

were traced with the aid of a camera lucida and the trace

lengths

measured with a cursor on a

_digitizing

table connected to a

_{microcomputer.}

_Except

for the obscura group

species,

the measure of

_cyst

_length

was

preferred

to that of sperm

length

to minimise the risk of

_breakage.

All details of this method are

_given

in

Joly

(1987

and

_1989).

The sperm

length

of the 48 other

species

belonging

to different taxa of the

Drosophilidae

are

_provided

in the literature

_(Sanger

&

_Miller,

1973;

Hatsumi

&

Wakahama,

1986;

Hihara &

Kurokawa,

1987).

RESULTS

Results for the

_investigated

_species

are

_given

in Table I and for the 13

_species

of the D. obscura group in Table III. Some of the

_species

_presented

in these tables have

already

been studied

_by

other

_{investigators,}

for

_example

D.

_melanogaster

_{(Table IV)}

and some

_species

in the D. obscura _group. Our measurements are, on the

_whole,

in

_good

_agreement

with

previous

data in

_spite

of

_{methodological problems}

_mainly

due to the

_difficulty

in

_obtaining

identifiable and unbroken cells. It is therefore

At a genus

level,

mean

_length

varies from 0.63

_(Amiota)

to 5.32 mm

(Myco-drosophila).

However,

among the 75

species

presently

studied,

64

belong

to the

Drosophila

genus which is itself characterized

by

a

huge interspecific heterogeneity.

A more detailed

_{analysis according}

to taxonomic subdivisions is

_presented

in the lower

_part

of Table II. The best documented

_{subgenera, Drosophila}

and

_Sophophora,

exhibit

_significant

_sperm

_length

_variations,

with means of 5.03 and 1.14 mm

respec-tively.

Also,

within each

_subgenus,

lower _taxa, i.e.

_species

_{groups, may} have different

lengths

and variations. For

_example,

in

_Drosophila,

flies in the D.

_immigmns

_group

have much shorter _sperm than in both the D.

_repleta

and D. _{virilis groups} which

are characterized

_by

_very

long

_sperm; the record

_length

is

_provided

here

by

D. lit-toralis from the latter _group where it reaches 2 _cm, that is 6 times the

_{body length}

(Table I).

In

_Sophophora,

we _may further contrast the D.

_medanogaster

and the D. obscura

_species

_{groups with} means of 1.45 and 0.30 mm

_{respectively.}

Another way of

analysing

the data is to consider the

_{heterogeneity}

among

species

belonging

to taxa of similar levels. Since mean

_lengths

are so

_variable,

variances cannot be used

_directly

and a relative _measure, the

coefficient

of variation

(c.v.)

has therefore been

_preferred.

This

_analysis

is limited to

_Drosophila,

since other genera are

_poorly

documented. On the other

hand,

the

_Drosophila

_genus

who

_recognized

_subgenera,

_species

_groups,

_species

_subgroups,

and within the

_latter,

species

complexes,

species

&dquo;clusters&dquo; ,

and

_pairs

or _groups of

_sibling

_species.

At _{the genus}

_level,

the overall c.v. is

130%

_{(Table II)}

which means that the standard deviation is

_higher

than the mean and the actual distribution is

_strongly

skewed towards

_high

values.

_Considering

lower level taxa leads to lower values of

c.v., i.e.

96%,

61%

and

34%

respectively

for

_subgenera,

_species

_{groups and}

_species

subgroups.

It _appears that

_homogeneity

increases when more

_closely

related

_species

are

_compared.

It has been shown that

_{intraspecific genetic variability}

in _sperm

_length

is

_poorly

species,

the

_shape

of the distributions of individual _sperm measurements is

_worthy

of

consideration,

and

_examples

of such distributions are

_given

in

_Figure

1. In D.

_melanogaster

and D. simulans the distributions are

obviously

unimodal and close to a

_gaussian

curve. Such is not the case in

_species

of _{the D. obscura group,} which exhibit clear-cut

_disjoint

distributions. This

_{intraspecific}

and intraindividual

heterogeneity

was

_already

known in some of these

_species

and the word

_polymegaly,

meaning

several

_sizes,

was coined to describe this situation

_(Beatty

&

_Sidhu,

1970;

Beatty

&

_Burgoyne,

_1971).

Our results confirm and extend these observations. In some _cases, such as D.

pseudoobscura,

it could be

argued that, by

visual

_inspection,

several

_peaks

may be

recognized.

However,

no statistical method exists for

_counting

the number of

_peaks

in a distribution. On the other

_hand,

visual

_inspection

_always

shows a well defined

_peak

for short _sperm while the situation _may be more

_complex

for

_longer

_sperm. As a conservative measure, it was decided to differentiate

_only

two size classes in each

_species,

i.e. short and

_long

sperm, the size limit between

size of mammals. The

_{interspecific}

_{variation ranges between 0.056 and 0.143} mm.

By

contrast,

the

_long

_sperm class is more

_{variable, ranging}

from 0.139 to 0.925 mm,

and is also more

_{heterogenous,}

as shown

_by

its

_high

c.v. When the two classes are

pooled,

the

_bimodality

of the distributions is evidenced

_by

the _very

_high

c.v. :

53%.

DISCUSSION AND CONCLUSION

The

_great

_length

of the _sperm of numerous

drosophilid

species

raises some technical

problems concerning length

determination: very

elongated

flagella

are

_easily

broken

during

dissection

_and,

_taking

into account

_{incomplete cells,}

would both decrease the calculated mean and increase the variance.

For that reason, measurement of mature

cysts,

assumed to

_give

more

reli-able

_data,

was

_preferred

in our

_study

for

_species

with

_longer

_{sperm, e.g.} in D.

!n,elanogaster.

This method in addition to the use of saline solution instead

of

previously published

(Table

IV).

For extreme

_lengths

of over one

_centimeter,

found

for

example

in D. littoralis.and D.

hydei,

even the

_cysts

are often broken so that it is _very difficult to evaluate

_{intraspecific}

_{variability. However,}

it seems reasonable to conclude that shorter values

_correspond

to

_incomplete

_cysts

and to consider

_only

the

_longer

measurements as

_typical

of the

_species.

In

contrast,

there are no technical difficulties in

having complete

short sperm

which do not break

_easily.

_Therefore,

the

_{heteromorphism}

of the distributions in the D. obscura _group

_species,

which has

_already

been observed

_{by previous}

investigators

(Yanders

&

_{Perras, 1960;}

_Beatty

&

_Sidhu,

_1970;

_Policansky,

_1970;

Beatty

&

_Burgoyne,

_1971;

_Sanger

&

Miller, 1973;

Kurokawa et

_al.,

₁₉₇₄₎

cannot be accounted for

_by

_any technical bias.

The occurrence of _very

_long

male

_gametes

in numerous

_Drosophila

_species

raises several

evolutionary questions,

to be discussed below. The first concerns the ancestral or

_primitive

state of sperm

length. According

to theories of modern

cladistic

systematics,

this may be inferred

by considering

taxonomic

_outgroups.

There are very few cases of animals with such

relatively giant

sperm.

Among

these are

featherwing

beetles

(Coleoptera, Ptiliidae) (Dybas

&

Dybas,

1981;

Taylor,

1982)

or some ostracods

(Bauer, 1940)

where sperm may be several times the male

length

(see

review in

_{Sivinski, 1984; Jamieson,}

_1987b).

_{Nevertheless, species}

_{with sperm}

of inordinate

_length

are still more common in fruit flies. A reasonable

proposal

is

therefore that short _sperm are

_primitive

while

long

_sperm are derived

(Hihara

&

Kurokawa,

1987).

However,

the situation is less clear at a lower

level;

in the D.

melanogaster).

Here if

_phylogeny

is considered

_{(Cariou, 1987)}

we must conclude

that

_elongation

occurred

_{independently during}

the

speciation

process. A similar

reasoning

could be

_applied

in

_comparing

other taxa in which there are

_species

with

either short or

_long

_sperm.

_{Unfortunately, knowledge}

of

_{Drosophila phylogenies}

does not

_presently

allow such

_comparison.

Whatever the conclusions

_might

_be,

it remains clear that evolution and

_speciation

in the

_{family Drosophilidae}

is characterized

_by

a

_{general tendency}

towards

_increasing

sperm

length,

as

_already

assumed

_by

Hihara & Kurokawa

_(1987).

This overall

_{evolutionary tendency}

further

_suggests

that size variation is not

random but has been

_subject

to natural selection

_{(Joly, 1989).}

The most

_important

questions

that then arise are: how and

_why

did sperm

elongation

evolve? Some

insights

may be

gained by considering

the

heteromorphism

of the D. obscura _group

species.

Clearly, heteromorphism,

which is

_typical

of the whole _{group, is}

_genetically

determined

_(Beatty

&

_Sidhu,

_1970).

_Moreover,

this does not

_correspond

to a

_genetic

polymorphism

at the

_diploid

_level,

since _any

_single

male

produces

heteromorphic

sperm. Nor is it a case of

_{gametic polymorphism}

since all the sperm

cells,

included in the same

_cysts,

and which could be

_genetically

_different,

exhibit the same

length.

Heteromorphism

seems to be more a case of

_{polyphenotypism}

which is determined

_by

some unknown

_{physiological}

mechanisms at the

_cyst

level. A reasonable

_{interpretation}

is that

_{heteromorphism}

is an

_evolutionary

stable

_strategy

(ESS) (Maynard

Smith,

1974),

each _sperm class

_having

some

_{adaptive advantage.}

For

_instance,

the short and

_long

_{sperm may} have differential

_capacities

both to reach

the

_storage

_organs

_{(preemption capacity)}

and to resist the second male

_paragonial

substances

_{(antipreemption capacity)}

when a female remates. A

_precise

formulation of such a

hypothesis,

which

_{requires comparison}

of the evolution of both _sperm

length

and

_mating

_systems

in different

_species,

is

_proposed

in a

_forthcoming

_paper.

REFERENCES

Afzelius

_B.A.,

Baccetti B. & Dallai R.

₍₁₉₇₆₎

The

_giant

spermatozoon

of Notonecta. Submicrosc.

_Cytol.

_8,

149-161

Alexander R.D. &

_Borgia

G.

₍₁₉₇₉₎

On the

_origin

and basis of the male-female

phenomenon.

In: Se!!aal Selection and

_Reproductive

_Competition

in Insects.

_(Blum

M.S. & Blums

_N.A.,

_eds),

Academic

_Press,

New

_York,

417-440

Baccetti B.

₍₁₉₇₉₎

Ultrastructure of sperm and its

bearing

on

arthropod

phylogeny.

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