Diversity effects in reproductive biology

Di 7 ersity effects in reproducti 7 e biology

Giorgina Bernasconi,Melanie Paschke and Bernhard Schmid,Institute for En7ironmental Sciences,Uni7.of Zurich,Winterthurerstr.190, CH-8057Zurich,Switzerland([email protected]).

In polyandrous species, such as most insects, the repro- ductive success of male parents is the outcome of competition via their gametes for resources that a fe- male has invested in her ova and will provide to the developing offspring (Parker 1970). Resource partition- ing among offspring and their genetic identity and diversity will also affect the reproductive success of female parents. These processes may be viewed as di- versity effects in reproductive biology, which parallel diversity effects in community ecology (Loreau et al.

2001). We suggest that the analysis of potential effects of multiple paternity, or in principle also of multiple maternity, on reproductive success in animals and plants could benefit from ideas and experimental de- signs that have innovated community ecology, espe- cially since diversity effects are being explored beyond the simple case of two or three interacting species (Kinzig et al. 2002, Loreau et al. 2002).

Recent experiments using randomly assembled plant communities ranging from 1 to over 10 species (e.g.

Hector et al. 1999) have shown that biomass produc- tion increases linearly with the logarithm of species richness. This finding has been explained by two poten- tial mechanisms referred to as ‘‘sampling’’ and ‘‘com- plementarity’’. Sampling occurs when a large initial number of species in a community increases the proba- bility that one or a few high-yielding species become dominant, thus resulting in high yield. Complementar- ity occurs for example when species differ in their resource requirements and therefore in combination extract more resources than a monoculture (or low-di- versity mixture). These mechanisms are not mutually exclusive. However, even if they occur together, their relative contribution to the observed diversity effects can be separated with analytical approaches related to the Price-equation in evolutionary biology (Loreau and Hector 2001, Hector et al. 2002).

Sampling processes

Do sampling and complementarity also occur when diversity is among sires in animals and plants, espe- cially where multiple paternity is not restricted to only two or three sires (Ellstrand 1984, Marshall 1991, Campbell 1998, Imhof et al. 1998)? The most obvious sampling effect in reproductive biology oc- curs among the many genetically related, yet usually not identical, male gametes of a single sire. In partic- ular, if the mother can only carry one offspring, then sperm competition is about getting all or none of the female ‘‘resources’’. More interesting sampling pro- cesses can arise through sperm or pollen competition among fathers in polyandrous matings of a female.

The larger the number or genetic diversity of male parents, the greater becomes the female parent’s chance to sample a particularly good single father for her offspring.

Indeed, polyandry, mate choice and postcopulatory sexual selection are considered to play important roles in reproductive biology (Birkhead and Møller 1998, Yasui 1998, Baer and Schmid-Hempel 1999, Birkhead and Pizzari 2002). In animals in which fathers con- tribute only genes, the advantages of sperm competi- tion and thus the benefits of polyandry to female fitness have been suggested in the opportunity to se- lect the best among several fathers (with heritably higher viability, fertilization ability, or attractiveness), or in the defence against genetic incompatibility (Zeh and Zeh 2001) including inbreeding (Tregenza and Wedell 2002; for the additional advantage arising from genetically diverse offspring, see next section).

In several taxa females re-mate more readily with novel partners (Archer and Elgar 1999). Furthermore, polyandry itself can intensify selection on sperm com- petitive ability (Bernasconi and Keller 2001, Hosken Published in Oikos 102, issue 1, 217-220, 2003

which should be used for any reference to this work 1

and Ward 2001), even leading to spectacular forms of altruistic cooperation among sperms of individual males (Moore et al. 2002). In flowering plants, where polyandry, due to the open pollination system, is prob- ably more common and more synchronous than in animals, the fusion of carpels (syncarpy) is one key innovation that intensifies pollen competition and thus increases the chances of obtaining pollen from the best male parent by the sampling process (Mulcahy 1979, Endress 1982). A recent phylogenetic analysis estimates that syncarpy has evolved independently 17 – 26 times in the flowering plants (Armbruster et al. 2002).

Complementarity processes

Sampling processes may occur more frequently in re- productive biology than in community ecology. This is because there are many more male gametes than will eventually be allowed to use the resources offered by the female parent, i.e. her gametes and her later support of developing offspring, whereas in community ecology most individuals and species, at least initially, have direct access to resources. However, a single female often produces many gametes and supports many off- spring, offering simultaneous access to male gametes from several male parents. It is thus conceivable that positive diversity effects in polyandrous species may also be due to processes involving complementarity.

First, genetic differences among female gametes within a maternal plant represent a ‘‘heterogeneous environment’’ which may best be ‘‘exploited’’ by a heterogeneous population of paternal gametes, if vari- ability among paternal gametes increases the chances for compatible and viable matches. Thus, differential matching of gametes to form fit zygotes constitutes one possible process (potentially involving both sampling and complementarity) leading to positive diversity ef- fects in reproductive biology. Second, even with a low genetic diversity of female gametes, a female could increase her fitness by mating with multiple males if this increases offspring diversity, leading to better resource exploitation in heterogeneous environments (Yasui 1998) or reduced sib-competition (Willson et al. 1987, Karron and Marshall 1990). The latter example would be the direct analogue to resource use complementarity reported from biodiversity experiments in community ecology (Hector et al. 2002). Under such a perspective potential fitness advantages for male parents of having offspring with many females (multiple maternity) might also be considered.

It is not obvious how to disentangle experimentally sampling and complementarity processes, but solutions have been found within community ecology and can be transferred to reproductive biology.

Analysing multiple-paternity as diversity effect

Most studies of sperm competition use 2-father matings (Birkhead and Møller 1998; for examples with 3-father matings see Zeh and Zeh 1994 or Lewis and Jutkiewicz 1998), rarely varying the genetic difference between fathers deliberately (Tregenza and Wedell 2002). This corresponds to early competition experiments in com- munity ecology which involved pure stands and two- species mixtures (de Wit 1960). General diversity effects were only detected when these experiments were ex- panded to larger ranges of species richness (Schmid et al. 2002). We suggest that a similar expansion of exper- imental designs should be considered for studies in reproductive biology. This should be particularly inter- esting for species with naturally high and variable num- bers of male parents for each single female (and vice versa). This situations most likely to plants with their open pollination systems or to animals (such as ascidi- ans and corals) with broadcast spawning and therefore the potential for simultaneous contribution of multiple mates to fertilization (Bishop 1998).

In a recent study using the rare plant Cochlearia ba6arica(Paschke et al. 2002), we observed a strongly positive log-linear effect of the number of pollen donors, increasing from 1 to 3 to 9, on female repro- ductive success (Fig. 1). Total pollen load was held constant in this experiment. The positive diversity effect is relevant for the survival of the study species, because it can overcome the observed bi-parental inbreeding depression in small populations (Paschke et al. 2002).

Although here the number of sires was greater than two, we do not know at present to which extent the effect of increased pollen diversity on reproductive suc- cess in C. ba6arica resulted from sampling or comple- mentarity. There are two additional requirements needed to disentangle the contributions of the two processes to diversity effects in reproductive biology, neither of which was fulfilled in our study. First, the proportion of the seeds of a maternal plant sired by each pollen donor or potential father should be mea- sured. This could be relatively easily done in species where genetic markers are available (see Ellstrand 1984 for an early example of a paternity analysis in plants).

Second, there is an experimental requirement, as in diversity studies in community ecology, namely that all fathers used in multiple-donor pollinations have also been tested in single-donor pollinations with the same female. If both requirements are fulfilled, methods us- ing the Price-equation (Frank 1995) or diallel analysis (Cockerham and Weir 1977, Mather and Jinks 1982) may be developed to separate the individual and com- bined contributions of particular fathers to the total reproductive success of a multiply sired female. These approaches have been used by Loreau and Hector (2001) and McGilchrist and Trenbath (1971), respec- 2

Fig. 1. Mean responses of seed set in 10 populations of Cochlearia ba6arica(Paschke et al. 2002) to pollination by an increasing diversity of pollen donors when the total amount of pollen is held constant (multiple regression analysis: log-linear effect: F1,9=13.88, pB0.005; deviation from log-linearity:

F1,9=0.052, p\0.1; population: F9,18=1.23, p\0.1). Er- ror bar: 1 SED=0.1184.

two males compete for a female’s ova in the same reproductive period under natural competitive situa- tions. Ideally, the number of sires should be varied below and above natural levels of polyandry (or polyg- yny) to explore the boundary of optimal mating rates (Baer and Schmid-Hempel 1999), which can differ be- tween males and females (Rice 1996). Furthermore, morphological, physiological, and genetic differences among sires may be varied in a next step (Tregenza and Wedell 2002), corresponding to the use of different levels of functional diversity in ecological biodiversity experiments (Schmid et al. 2002). Perhaps, integrating concepts and methods from different fields and across different levels of biological organisation will eventually lead towards a general theory of diversity.

Acknowledgements – We thank Scott Armbruster, Andy Hec- tor, Barbara Hellriegel, Michel Loreau, Owen Petchey and Io Skogsmyr for valuable comments on earlier versions of this paper, and the Swiss National Science Foundation (Swiss Priority Programme Environment, no. 5001 – 44628), Swiss Federal Program for Academic Recruitment (No. 409) and Forschungskredit der Universita¨t Zu¨rich (No. 560065) for financial support.

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Conclusion

Over the past three decades experiments in reproductive biology have explored the case of double mating, providing detailed insights into mechanisms affecting paternity in a variety of taxa (Birkhead and Møller 1998). We suggest that additional progress could be made by transferring to reproductive biology concepts and analysis methods developed in community ecology for effects of species diversity. In particular, two poten- tial processes, sampling and complementarity, may sim- ilarly explain effects of multiple paternity or maternity on the fitness of individuals as they explain effects of species richness on the performance of communities (Loreau et al. 2001). New experiments in reproductive biology should be designed to vary the numbers of sires over a larger range. Indeed, in many species more than

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