sex hermaphrodites

8/13/2019 Sex Hermaphrodites

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Sex in Simultaneous Hermaphrodites

Lukas Schrer

Evolutionary Biology

Zoological Institute

University of Basel

27.11.2013 Advanced-level Evolutionary Biology

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Mating in the leopard slug (Limax maximus)

from the BBC nature documentary Life in the Undergrowth


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distribution of hermaphroditism

advantages of hermaphroditism sexual selection

Batemans principle

male and female cross-terms

sexual conflict

conditional egg trading in the hamlets

conditional sperm exchange in internal fertilisers

cryptic female choice

rejection or digestion of received sperm

sperm trading

bypassing female control (hypodermic impregnation)

manipulation of cryptic female choice

preventing the partner from mating again

Summary: Sex in Simultaneous Hermaphrodites

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hermaphroditism occurs in about 70%(24 of 34) animal phyla

it is frequent or dominant in 14 phyla

the 10 purely gonochoristic phyla containrelatively few species

only 5-6% are hermaphrodites (30% wheninsects are excluded)

hermaphroditism is rare in vertebrates

there is a strong phylogenetic componentin the distribution

Distribution

modified from Jarne & Auld 2006

Ph lum S ecies Herma hrodites

Placozoa 1

Demos on ia 8000

Hexactinelida 1000

Calcera 1000

Cnidaria 9000

Cteno hora 100

M xozoa 1200

Rotifera 1800

Acanthoce hala 1150

C clio hora 1

Ento rocta 150

Plat helminthes 13780

Nemertini 900

Mollusca 117495

Si uncula 320

Annelida 14360

Ecto rocta 4500

Brachi oda 335

Phoronida 15

Chaeto natha 100

Gastrotricha 430

On cho hora 80

Tardi rada 600

Arthro oda 956414

Nematoda 20000

Nemotomor ha 325

Kinorh ncha 150

Loricifera 9

Pria ulida 16

Mesozoa 50

Echinodermata 6000

Hemichordata 85

Urochordata 1300

Vertebrata 50911

frequent or dominant

relatively rare

absent


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reproductive assurance (Darwin 1876)

if one does not find a partner, one can still self-fertilise

but many simultaneous hermaphrodites actually do not self-fertilise

low density (Tomlinson 1966, Ghiselin 1969)

every partner you meet is a potential mating partner

local mate competition (Charnov 1979, Charnov 1982)

limited male-male competition

local sperm competition (Schrer 2009)

competition between related sperm

!these factors generally favour a female-biased sex allocation

Advantages

6Schrer Evolution 2009

Fischer 1981Charlesworth & Charlesworth 1981

Charnov 1980Charnov 1982

Greeff et al. 2001

Charnov 1996

Van Velzen, Schrer & Pen 2009

Advantages


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simultaneous hermaphrodites probably often have a higher femalethan male investment

!the fitness return per unit of male investment is higher

Advantages

ovotestis of the Barred Hamlet(Serranidae: Hypoplectrus puella)

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Sexual selection

Darwin (1871) doubted that sexual selection occurs insimultaneous hermaphrodites

with animals belonging to the lower classes, the two sexes are not rarely unitedin the same individual, and therefore secondary sexual characters cannot bedeveloped [...] Moreover it is almost certain that these animals have tooimperfect senses and much too low mental powers to appreciate each other'sbeauty or other attractions, or to feel rivalry

but Darwin was only aware of pre-copulatory sexual selection

there is little evidence for traits involved in pre-copulatory sexual selection;most sexual selection appears to be post-copulatory (i.e. sperm competition andcryptic female choice)

Parkers (1970) recognition of sperm competition paved the way to a betterunderstanding of sexual selection in hermaphrodites


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Batemans principle

in a female, reproduction tends to be limited by the number (and quality) of eggsshe produces, which is often limited by the amount of resources she has

in a male, reproduction tends to be limited by the number (and quality) of eggshe fertilises, which is often limited by the number of females he can mate with

!males will tend to want to mate more often than females

eager males and choosy females

sexual conflict between males and females over the optimal mating rate

Sexual selection

Bateman 1948

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Charnov (1979) was the first to explicitly consider Batemansprinciple in simultaneous hermaphrodites

I propose here that Bateman's principle is also valid for these organisms thatfertilized egg production by an individual is limited not by the ability to getsperm, but by resources allocated to eggs. This is a strong assumption [...].However, if it is approximately true, then [this] has several importantimplications for reproductive biology

!hermaphrodites will tend to prefer mating in the male sex role

simultaneous hermaphrodites often mate to give, rather than receive, sperm

sexual conflict between the sperm donor and sperm recipient should be intense

Sexual selection


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Chain and ring mating in sea slugs

Aplysia dactylomela Chelidonura punctata

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an individuals male and female mating success may not be independent

Sexual selection

Anthes et al. 2010


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an individuals male and female mating success may affect its male andfemale reproductive success differently

Sexual selection

Anthes et al. 2010

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in a gonochorist a mated female may not want to engage inadditional copulations

if she has enough received sperm to fertilise her eggs and if additional matingsoffer no advantage

avoiding males avoids (at least some) sexual conflicts

Sexual conflict


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the female function of a mated hermaphrodite may not want toengage in additional copulations

if it has enough received sperm to fertilise its eggs and if additional matings offerno advantage

thus the female function may want to avoid additional matings

but the male function of the same individual will want to continueto mate

Sexual conflict

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thus if two mated simultaneous hermaphrodites meet they mayhave incompatible mating interests

both individuals may want to donate, but not receive, sperm

mating should take place if the net benefit for mating is positive

this can occur even if there is a cost to one sex

a possible solution is reciprocal mating where acceptance of spermreceipt is conditional on sperm donation

this is expected to lead to sexually antagonistic coevolution (asexual arms-race) between

adaptations in the recipient that allow to remove (or otherwise control) spermreceived in such matings (a form of cryptic female choice)

counter-adaptations in the donor that prevent sperm removal by the recipient (aform of male persistence)

Sexual conflict


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sexual conflicts over the mating role

17Michiels 1998

Sexual conflict

compatible

incompatible

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egg trading in the hamlets (Hypoplectrus spp.)

both individuals should prefer to fertilise the eggs of the partner

they solve this by alternately assuming the male and female role

barred

black

shy

blue

golden

butter

masked

indigoovotestis of Hypoplectrus puella

Sexual conflict


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vMichiels 1998Michiels 1998

mating in Hypoplectrus puella

Fischer 1980

Sexual conflict

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how do they prevent cheating?

check, and if necessary, punish your partner!

checking the partner is easier with external fertilisation

Sexual conflict

Fischer 1980


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conditional sperm receipt

in order to donate sperm one also has to accept their receipt

!simultaneously reciprocal mating behaviour

Archaphanostoma agile(Acoela)

Monocelis fusca(Proseriata)

Lumbricus terrestris(Oligochaeta)

Deroceras sp.(Pulmonata)

Sexual conflict

Mating behaviour inMacrostomum lignano

22Schrer et al. 2004


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simultaneously reciprocal mating behaviour:

is sperm acceptance really conditional on donation?

available data do not allow to test this

does this lead to fertilisation trading?

the little available data suggest that not

what do you do with sperm you did not want?

cryptic female choice by control, rejection or digestion

Sexual conflict

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storage tubules for sperm of different sperm donors in the free-living flatwormParomalostomum dubium?

Sexual conflict

Rieger 1971


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Mating behaviour inMacrostomum lignano

26Schrer et al. 2004


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sperm digestion

connection between sperm-receiving organ and the gut in the free-living

flatworm Promacrostomum paradoxum(Platyhelmithers: Macrostomidae)

Sexual conflict

An-der-Lan 1939

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conditional sperm donation

with efficient cryptic female choice sperm donation !fertilisation

if most sperm is digested, mating in male role can become costly

sperm donation can become conditional on sperm receipt (only

mate with partners that are are also willing to invest a lot)!conditional sperm trading in a planarian flatworm

Vreys & Michiels 1998

Dugesia gonocephala(Platyhelminthes: Tricladida)

Sexual conflict


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an experimental test of the conditionalsperm trading hypothesis in a sea slug

a cauterised individual can not donate sperm, andis thus forced to cheat

the focal individual reciprocates fewer copulationsto a cheater than a control

the focal individual deserts cheaters more oftenthan controls

but an alternative explanation is choice against asick partner

Anthes et a. 2005

Sexual conflict

Chelidonura hirundinina(Gastropoda: Cephalaspidae)

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hypodermic sperm donation

allows to avoid receiving sperm (and any costs required tocontrol such received sperm)

allows to bypass cryptic female choice (even if hypodermicfertilisation is not very efficient, it may still be better)

Pseudaphanostoma psammophilum

(Acoela)

Pseudoceros bifurcus

(Platyhelminthes: Polycladida)

Sexual conflict

Michiels & Newman 1998


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penis fencing in Pseudobicerossp. (Platyhelminthes: Polycladida)

Sexual conflict

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hypodermic sperm donation inMacrostomum hystrix

Sexual conflict


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hypodermic sperm donation inMacrostomum hystrix

Sexual conflict


the function of the love dart in pulmonate snails

Sexual conflict

The love-dart (D) is produced and stored in the stylophore

(S, often called dart sac) and shot by a forceful eversion ofthis organ. The mucus glands (MG) produce the mucus that isdeposited on the dart before shooting. The penis (P) isintromitted to transfer the spermatophore. The spermcontainer is formed in the epiphallus (EP), while thespermatophore's tail is formed by the flagellum (FL). When abursa tract diverticulum (BTD) is present, the spermatophoreis received in this organ. Together with the bursa tract (BT)and bursa copulatrix (BC) these form the spermatophore-receiving organ (SRO, indicated in grey), which digest spermand spermatophores. Sperm swim out via the tail of thespermatophore to enter the female tract and reach thesperm storage organ (SP, spermathecae) within thefertilization pouch (FP)-spermathecal complex. Otherabbreviations: AG, albumen gland; G, genital pore; HD,

hermaphroditic duct; OT, ovotestis; PRM, penis retractormuscle; SO, spermoviduct; V, vaginal duct; VD, vas deferens.

Koene & Schulenburg 2005


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the function of the love dart in pulmonate snails

Sexual conflict

Chase & Blanchard 2006Koene & Chase 1998


morphological diversity of the love dart

Sexual conflict



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evolution of the love dart

Sexual conflict



coevolution between male and female traits

Sexual conflict



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Sexual conflict

preventing the partner from mating again

can target the male or female function

e.g. penis biting in banana slugs,Ariolimax (has only rarely been observed)

Reise & Hutchinson 2002

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distribution of hermaphroditism

advantages of hermaphroditism

sexual selection

Batemans principle

male and female cross-terms

sexual conflict

conditional egg trading in the hamlets

conditional sperm exchange in internal fertilisers


rejection or digestion of received sperm

sperm trading

bypassing female control (hypodermic impregnation)

manipulation of cryptic female choice preventing the partner from mating again

Summary: Sex in Simultaneous Hermaphrodites


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Literature

Mandatory Reading

none

Suggested Reading

Michiels (1998). Mating conflicts and sperm competition in simultaneoushermaphrodites. Pp. 219-254 in Birkhead, and Mller, eds. Sperm Competitionand Sexual Selection. Academic Press, London, England.

Chapter 6 in Arnqvist & Rowe (2005). Sexual Conflict. Monographs in Behaviourand Ecology. Princeton, NJ, USA: Princeton University Press.

Books

Avise (2010). Hermaphroditism: A Primer on the Biology, Ecology, and Evolutionof Dual Sexuality. New York, NY: Columbia University Press.

sex hermaphrodites

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