Encyclopedia of Evolutionary Biology

Exclusive Preview Articles

Page 2 - Preface Page 3 - The Evolutionary Ecology of Mutualism Page 10 - Recombination and Molecular Evolution Page 16 - Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth PREFACE

The Encyclopedia of Evolutionary Biology was developed to pro- Smocovitis and Norman Johnson) cover the history of evo- vide an authoritative overview of the current state of evo- lutionary biology and applications of evolutionary biology. lutionary biology. It was an ambitious goal, especially given Readers of the encyclopedia will find that entries are gen- that the field did not pause for the two and a half years needed erally pitched at a somewhat advanced level, although with to complete the project. The encyclopedia’s 15 section editors great effort by authors to make entries as accessible as possible collaborated to ensure that content gaps were kept to a min- to a broad audience. Encyclopedias, like living organisms, are imum, and their efforts show. When the project was com- compromises. If all entries could be readily understood in pleted, we had compiled 256 entries, covering a broad range their entirety by first-year university students, this encyclopedia of topics selected by the editors to ensure a comprehensive would be of limited value to experts. At the other extreme, resource. It was a privilege to read every one of these entries, if entries were extremely technical – and our authors were and I was truly humbled by the collective efforts of hundreds undoubtedly capable of producing such entries – the en- of authors to communicate the excitement and sophistication cyclopedia might be inaccessible to students. While there is, by of a field of study that touches on every conceivable topic necessity, variation among entries in this regard, we settled on in biology today. a general target: the majority of an entry should be accessible There are many ways to envision an encyclopedia of evo- to a motivated, advanced undergraduate. Readers are, of lution, and we had to choose an approach that would lead course, directed to additional resources, with authors pro- to a cohesive resource. Readers will note that, in the more viding bibliographies and lists of further reading. organismal-focused entries (edited by David Guttman, Amy As with any undertaking of this scale, there are many Litt, and Claudia Russo), there is an emphasis on diversification individuals who should be recognized for their roles in of life. We did not set out to provide an overview of the the development of this encyclopedia. Special thanks go to diversity of life, as such a goal would be untenable; rather, Norman Johnson for early discussions that helped us develop we focused on the evolutionary processes and key events the general structure of the encyclopedia. The dedicated and responsible for diversity. Numerous entries deal with speci- distinguished team of section editors deserves the credit for ation, life history evolution, evolutionary biogeography, and drafting the table of contents, recruiting authors, and working coevolution. These entries (edited by Daniel Ortiz-Barrientos, extensively with authors to ensure the highest quality product. Tim Coulson, Rosemary Gillespie, and Andrew Forbes) bring It should go without saying that the high quality of this en- to light how the evolution and diversification of life is cyclopedia ultimately reflects the efforts of the editors and intimately entwined with ecology. Of course, there is extensive authors. Finally, the project management and development coverage of population genetics, quantitative genetics, evo- teams at Academic Press were always ready to assist, and lutionary developmental biology, the evolution of sex and while it is not possible to name everyone who contributed to mating systems, molecular/genome evolution, and phylo- the effort, I am particularly indebted to Simon Holt, Will genetic analysis (edited by Maria Orive, Jason Wolf, Karen Bowden-Green, Paula Davies, and Justin Taylor. Sears, Nina Wedell, Hiroshi Akashi, and Laura Kubatko), all fundamental to our understanding of evolutionary processes. Richard Kliman And as thematic bookends, several entries (edited by Betty Editor in Chief

xxxi Mutualism, the Evolutionary Ecology of DM Althoff and KA Segraves, Syracuse University, Syracuse, NY, USA r 2016 Elsevier Inc. All rights reserved.

Glossary individuals of the other species and in return receives By-product mutualism An association among species in nutrients or resources needed for growth and reproduction. which the resources exchanged are cost free to at least one Exploiter A species from outside a mutualistic interaction partner and are produced as by-products of other that takes the resources or services provided by mutualistic organismal functions such as metabolism. species without providing anything in return. Cheater An exploiter species that evolved from a Geographic mosaic of coevolution The concept that most mutualistic one and no longer reciprocates with its partner. of the coevolution among species occurs at different rates in Coevolution Reciprocal evolutionary change caused by an different populations with some populations being interaction among species. hotspots of coevolutionary change. Coevolutionary hotspot Populations where all interacting Host sanctions A mechanism by which a mutualist can species are evolving in response to one another. reduce the trade of resources or services in response to a Connectedness In a community of interacting mutualists, partner that is of inferior quality. connectedness is the proportion of the total possible Nutritional mutualism An interaction among species in interactions among species that are observed within an which partners exchange nutrients needed for growth and interaction network. reproduction. Cooperation The act of individuals working together for a Partner choice A mechanism by which mutualistic common benefit. Mainly applied to interactions among partners preferentially interact with high-quality partners. individuals within the same species. Partner fidelity feedback Mutualisms where the increase Defensive mutualism An interaction among partner in fitness of one mutualistic partner causes an automatic species in which one partner defends the other in exchange increase in the other resulting in a positive feedback loop. for a place to live or for nutrients needed for growth and This is usually only possible between individuals of reproduction. different mutualist species that associate long enough to Dispersive mutualism An interaction among species in experience changes in fitness. which one partner moves the gametes, offspring, or

Introduction can apply to mutualistic interactions, but not all mutualisms include cooperation or facilitation, and not all symbioses are Species interact with one another in myriad ways with the mutualisms. ultimate goal of obtaining resources or services needed for Mutualistic interactions are traditionally divided into three survival and reproduction. Many of these interactions are an- different types based on the resources or services that are tra- tagonistic in which one species gains a benefit but the other ded between species. Nutritional mutualism involves inter- suffers a cost. Predators, herbivores, and parasites either kill actions among species that are trading resources that are their hosts for energy and nutrients or take some resources needed for growth and reproduction. A classic example is the directly from their hosts. In contrast, there are interactions in trade of carbon and minerals between plants and mycorrhizal which the species involved all gain reciprocal benefits. Van fungi. Plant roots form intimate associations with the hyphae Beneden (1873) was the first to call these interactions mutu- of fungi that are very fine and can forage efficiently for phos- alisms. For example, bees visiting a flower gain energy from phorus, nitrogen, and micronutrients in the soil (Courty et al., nectar rewards while providing pollen exchange for the plant. 2010). The roots exude rich carbon compounds that are used Since the term was coined, we have come to realize that as food by the fungi which in return provide the plant with mutualisms are the foundation of most ecosystems (Figure 1). scavenged water and minerals. Dispersive mutualism involves For instance, in terrestrial systems, plants interact with a variety one partner species distributing gametes, offspring, or indi- of species that help in the procurement of nutrients, the dis- viduals of another species in return for a resource. The persal of pollen and seeds, and defense against herbivores. In diversification of angiosperm plants is partly attributed to their aquatic systems, coral and their symbiotic algae build the ex- mutualism with pollinating insects that act as directed pollen tensive reef ecosystems that harbor much of the ocean’s bio- dispersal agents (Grimaldi, 1999). Likewise, plants also often diversity. Furthermore, mutualisms involve a taxonomically trade food rewards with a diversity of mammals, birds, and diverse set of species, occur in every environment, and occur insects that inadvertently disperse plant seeds. Lastly, defensive among highly mobile free-living species as well as those that mutualism involves one species defending another in ex- live on or within other species. For this reason, many add- change for resources and/or a place to live. For example, itional terms have been synonymized with mutualism such as ants protect acacia plants from herbivores such as elephants in cooperation, facilitation, and symbiosis. Each of these terms exchange for nesting locations within the tree and packets of

Encyclopedia of Evolutionary Biology, Volume 3 doi:10.1016/B978-0-12-800049-6.00187-6 87 88 Mutualism, the Evolutionary Ecology of

(a) (b)

(c) (d)

Figure 1 Examples of mutualisms. (a) Eastern deciduous forest in central New York, USA highlighting young maple seedlings that will need to establish mutualistic interactions with ectomycorrhizal fungi. (b) Coral reef in the British Virgin Islands. (c) Fruiting body of ectomycorrhizal fungus species at the Archbold Biological Station in Florida, USA. (d) A species of bombyliid fly nectaring on a flower in central Florida, USA. proteins produced by specialized leaves (Goheen and Palmer, both mutualists (Frederickson, 2013). In considering the ori- 2010). gin of mutualism, a poignant question to address is whether Regardless of the type of mutualism, there are a variety of the interactions were mutualistic from the beginning or did ecological and evolutionary factors that influence the for- they gradually transition into mutualism over time. If it is the mation and continued functioning of the interaction. As a former, what conditions favor this scenario? If it is the latter, consequence, research in mutualism is focused on answering how do some antagonistic interactions eventually change into at least four major questions (Bronstein et al., 2006). The first mutualistic ones? Additionally, are traits important to mutu- is to understand how mutualism originates. Why do species in alistic interactions co-opted from existing traits or must novel essence hitch their futures together by relying on one another traits evolve de novo? for goods or services? The second major question is: How is Determining the origin of mutualism is a difficult process, mutualism maintained among species that are under constant especially given that interaction outcomes can change de- selection to obtain resources from their partners while re- pending on the environmental context. Addressing this ques- ducing the cost of reciprocating? Why don't the partners cheat tion also requires combining information on the phylogenetic and reduce their costs? The third major question is: Why are history of the species involved and the dynamics of the inter- some mutualistic interactions very specialized and involve, in action and the traits important for the mutualism (Sachs et al., some cases, just a pair of species and in other cases involve 2014). Some of the best evidence for how mutualism originates several or even dozens of other species? Finally, given that comes from studies of yuccas (Asparagaceae: Agavoideae) and mutualism is the foundation of many communities, how does their pollinating moths. Moths in the family Prodoxidae are the addition of other community members that interact with plant feeders in which the larvae feed internally on plant tissues, mutualist species influence the dynamics of mutualism? either in the leaves, flowering stalks, or within developing fruits (Davis, 1967). Phylogenetic analysis of the three closely related prodoxid genera that feed on yuccas, Prodoxus, Parategeticula, The Origin of Mutualism and Tegeticula, reveals an interesting progression of the overall interaction from antagonism to mutualism (Figure 2). Many of the mutualisms we observe today are likely the Prodoxus moths colonized yuccas as herbivores and product of a long-term process of adaptation among one or diversified to feed within galls on the leaves, within the Mutualism, the Evolutionary Ecology of 89

8 7 Eggs placed shallow 6 Tegeticula Eggs placed deep 3, 4 within flower Major steps in moth evolution 5 Larvae burrow 8 Evolution of two cheater species Parategeticula into flower

7 Eggs placed just under surface 2 6 Eggs placed deep in flowers

5 Eggs placed near flowers Fruit feeders

4 Seed feeding 1 Inflorescence stalk 3 Active pollination and leaf feeders Prodoxus 2 Yuccas colonized Stalk and fruit feeders 1 Eggs placed within plant tissue

Outgroup Figure 2 The evolutionary transitions between antagonism and mutualism in the yucca moth genera, Prodoxus, Parategeticula, and Tegeticula. Numbers along the branches correspond to major evolutionary changes in moth biology. Top right picture shows a female Tegeticula using the special ‘tentacles’ to actively deposit pollen into a yucca flower. Adjacent picture shows a larva and its feeding damage to the developing seeds. Bottom right picture shows a Prodoxus female laying eggs into a yucca flowering stalk. The larvae feed with the stalk and tunnel through the plant tissue.

flowering stalk, or within galls on developing fruit of yuccas to mutualism in the case of Parategeticula. The only reason that (Pellmyr et al., 2006). A female Prodoxus deposits her eggs into the outcome of the interaction between yuccas and Para- the plant tissue during the flowering season of her host plant tegeticula is considered a mutualism, however, is because the species and the larvae develop internally, feeding on host plant larvae only consume a small subset of the seeds in the yucca tissue, but never on seeds. The interaction between Prodoxus flower that their mother pollinated. The plant loses some seeds and yuccas likely ranges from neutral to slightly antagonistic as to the larvae, but experiences an overall positive fitness in- larval feeding does not seem to impact plant reproductive crease due to the pollination by the female moths. This overall success much (Althoff et al., 2004). Like some Prodoxus species, interaction highlights a very important dynamic of mutualism Parategeticula moths also feed within galls on developing fruit, – there is always some level of antagonism involved and it is but unlike Prodoxus, the galls encompass a small portion of the the relative increases and decreases in fitness that determine developing yucca seeds that the larvae also consume (Powell, whether we call an interaction an antagonism or a mutualism 1992). A Parategeticula female scrapes shallow pits into which (Bronstein, 1994). If we just considered larval feeding, Para- she deposits her eggs in the flower pedicel or the small side tegeticula reduces yucca fitness much more than Prodoxus that branches holding the flowers. The larva then crawls to a flower do not feed on seeds. The evolution of active pollination, and burrows into the base of the pistil to initiate a gall that likely as a result of selection on female moths to increase their replaces a few yucca seeds. Up to this point, the interaction offsprings’ survival, was the key event that shifted the outcome would be considered antagonistic as moth larvae are killing of the overall interaction. The effectiveness of active pollin- potential plant offspring. However, the female Parategeticula ation by Parategeticula also likely selected for the loss of other also pollinates the flowers near where she deposits her eggs. pollinators of yuccas. Yucca flowers produce no nectar and This action increases the probability that the flowers will de- there are no other known pollinators except for a single case of velop into fruit in which the larvae can feed and develop. To an introduced yucca in the United States, Yucca aloifolia, that is accomplish pollination, a female uses a completely novel trait inadvertently pollinated by honeybees (Rentsch and Leebens- – specialized mouthparts called tentacles – to collect yucca Mack, 2014). Thus, the interaction between moths and plants pollen into a ball that she carries beneath her head and to has become highly specialized and absolutely critical to the actively deposit some of the pollen into the stigmatic cavity of evolutionary success of both lineages. the yucca flower (Davis, 1967). Because a female moth Evolution within the moth genus Tegeticula further high- transfers enough pollen to fertilize many more seeds than her lights the ongoing dynamic of antagonism within mutualism. offspring will eat, the net outcome for the plant is positive. The This genus contains over 17 species of pollinator moths, but plant loses a small subset of its seeds to the moth larvae, there has also been the evolution of at least two cheater species but gains many more through active pollination by a highly (Pellmyr, 1999). These cheater species no longer pollinate and specialized and efficient pollinator. accordingly have even lost the tentacles, yet the larvae still feed In Parategeticula, there has been a switch in the outcome on yucca seeds. Like Parategeticula females, a female Tegeticula of the interaction from antagonism, as in the case of Prodoxus, pollinates flowers but pierces through the locule wall and 90 Mutualism, the Evolutionary Ecology of deposits her eggs next to the developing plant ovules rather bacterium might produce a waste product that is excreted into than in shallow pits outside of the flower. Egg and larval the environment. Once excreted, the by-product can be con- survivorship is likely increased because the eggs are protected sumed by other bacterial species that require it. There are inside of the flower. The tradeoff, however, is that the female’s many examples of cross-feeding in microbes where partner ovipositor damages some of the developing ovules. If there are species trade excreted products (Bull and Harcombe, 2009; many oviposition attempts on a single flower, the ovule Mee et al., 2014). damage triggers floral abscission and kills the eggs/larvae. Second, a similar mechanism that can stabilize mutualistic Within Tegeticula, another lineage of moth species evolved interactions is partner fidelity feedbacks. In this model, the probably in response to this floral abscission mechanism. resources being traded are costly; however, there is a direct link In this second lineage, females lay their eggs superficially between the amount invested in the mutualism and the just under the style or pistil surface. This placement prevents benefits received (Weyl et al., 2010). That is, individuals that ovule damage and potentially allows females to lay many eggs invest more in providing benefits to their partner will enhance (Segraves, 2008). From within this superficially egg laying the productivity of their partner and automatically receive lineage arose the antagonistic cheater moths. There are two more benefits in return. An example of a partner fidelity cheater species that lay eggs into early fruit or late fruit and do feedback is the interaction between plants and mycorrhizal not pollinate. These species are capitalizing on the remaining fungi that live in plant roots. Plants that invest in carbon to seed resource that would not be eaten by the pollinator larvae. roots infected with fungi increase growth of fungal hyphae that Thus, within the yucca moths, the interaction with yuccas has forage for nutrients in the soil. By doing so, the plants gain shifted from antagonism to mutualism and back to antagon- nutrients and can in turn grow and invest more carbon to ism, even though all moths feed on yuccas. fungi. The feedback continues with each partner receiving increased benefits as they trade resources. A third regulatory mechanism that can prevent over- The Maintenance of Mutualism exploitation by mutualist partners are host sanctions where one or both mutualist partners ‘punish’ partners that defect As evidenced by the evolution of cheater moth species in the from the mutualism. A clear example of host sanctions is yucca–yucca moth system, mutualism can be the target of the mechanism by which yuccas use to regulate the number of exploitation, both from within mutualistic lineages and from pollinator moth eggs placed within flowers (Pellmyr and without (Yu, 2001). Indeed, the prevention and mitigation of Huth, 1994). Some female yucca moths use their ovipositors exploitation has played a significant role in directing empirical to deposit eggs next to the developing seeds, and as they do so, studies and in the development of mutualism theory. Two they often damage the ovules and surrounding tissue. Yuccas types of exploitation have been distinguished. The general selectively abscise flowers with large numbers of wounded term ‘exploiter’ refers to organisms that take the benefits of ovules, killing all eggs/larvae within them (Marr and Pellmyr, a mutualism without offering anything in return; thus, ex- 2003). As a result, yuccas can sanction female yucca moths ploiters can be opportunists from the community or they can that lay so many eggs that no seeds would survive. originate from the mutualism itself (Sachs and Simms, 2006). Finally, partner choice mechanisms regulate mutualisms by The term ‘cheater’ specifically refers to an exploiter that is allowing mutualists to choose among partners that vary in evolutionarily derived from a mutualist lineage. Cheaters quality (Bull and Rice, 1991). Mutualists should associate could be mutant mutualists that no longer provide a reward more often with partners that provide the most benefits, thus or, as in the case of yucca moths, they could be entirely dif- reducing the costs of the interaction. The mutualism between ferent species that evolved from a mutualistic ancestor. The cleaner wrasse and their ectoparasite-riddled fish hosts is an presence of exploitation in mutualism presents an evolution- excellent example of partner choice. Host fish visit cleaning ary paradox. The reasoning is simple: because mutualisms stations where cleaner wrasse feed on the ectoparasites; how- generate resources that are often costly to make, individuals ever, sometimes the cleaners also bite healthy host tissue. that can obtain these benefits without reciprocating will be Repeated interactions between hosts and cleaners allow the favored by natural selection. Thus, exploiters of mutualism hosts to selectively visit cleaners that remove ectoparasites avoid the costs of participating in the interaction yet are able to without biting healthy tissue (Bshary and Schaffer, 2002). obtain the benefits that enhance fitness. Natural selection, Even with these mechanisms in place, exploitation is a then, should favor exploitative individuals that maximize common facet of mutualism. For example, cheater yucca the benefits while reducing the costs, potentially leading to moths do not pollinate, yet lay eggs into yucca fruit and their mutualism breakdown. larvae feed on seeds. Many flowering plant species produce A long-standing question in the study of mutualism is to conspicuous flowers that contain a nectar reward that entices understand how mutualists prevent their partners or other potential pollinators to visit the flower and inadvertently organisms from overexploiting the benefits of the mutualism. transfer and pick up pollen. Numerous pollinator species, Theoretical work has identified four general ways that mutu- however, will also sometimes cut through the base of the alisms remain stable: by-product mutualisms, partner fidelity flower to rob the nectar (Irwin and Brody, 1998), or are not feedbacks, host sanctions, and partner choice. First, by-product morphologically adapted to be good pollinators, so they feed mutualisms remain stable because one or both partners pro- on nectar without providing the pollen transfer service. Simi- duce a cost-free by-product. The release of the by-product larly, some frugivores (fruit feeders) are poor seed dispersers directly benefits the individual producing it, and as a con- because the plant seeds are damaged or killed during passage sequence, there is no incentive for exploitation. For example, a through the digestive tract. Further empirical and theoretical Mutualism, the Evolutionary Ecology of 91 studies are needed to clarify whether the costs of exploitation The Community Context of Mutualism are normally high or whether exploitation is more likely to have a minimal effect on a mutualistic interaction. The wide- Irrespective of whether a particular mutualism is specialized or spread prevalence of exploiters suggests that it might be the generalized, the biological reality is that all mutualisms are latter (Bronstein, 2001). embedded in communities of interacting species. These species interact directly or indirectly with mutualists, and so may have the potential to influence the evolutionary ecology of the Mutualism, Specialization, and Coevolution mutualism (Stanton, 2003). The study of mutualism is ex- panding to explore how not only other mutualist species but Another important facet of mutualism is that natural selection also how herbivores, natural enemies, and competitors of can favor the continued interaction of mutualists throughout mutualists may shape both the dynamics and the evolution of time. Because of this, mutualists can end up being specialized mutualistic traits (Afkhami et al., 2014). As mentioned earlier, through local adaptation to their partner(s). Hand in hand with the mutualism between yucca moth pollinators and yuccas is this specialization, is the process of coevolution in which there highly specialized, yet both moth and plant species have to is reciprocal evolutionary change among species. For example, contend with other visitors that feed on the flowers of yuccas. the long nectar spurs of Madagascan orchids result in the ex- The inflorescences of Yucca filamentosa populations in the tremely long proboscis of its hawkmoth pollinators (Arditti southeastern United States attract the pollinator moth Tegeti- et al., 2012). A similar pattern is observed among populations cula cassandra as well as large numbers of the pollen-feeding of the flowering scroph Zaluzianskya microsiphon (Scrophular- beetle Hymenorus densus and the plant fluid feeding leaf-footed iaceae) and its long-tongued fly pollinator Prosoeca ganglbaueri bug Leptoglossus phyllopus (Althoff et al., 2013). Feeding by (Diptera: Nemestrinidae) in South Africa (Anderson and these two species can cause severe damage to yucca flowers Johnson, 2007). In this example, the length of the floral tube and cause them to abscise from the plant. Thus, pollinator for the plant is highly correlated with the length of proboscis of moths have to contend with additional egg and larval mor- the fly across many different populations. Thus, specialization tality that may influence the pattern of egg deposition both and coevolution can occur both within and among popu- within a single plant and across many different plants. lations or across species in interacting lineages (Thompson, Furthermore, the effect of the beetle H. densus is even more 1994). In particular, the geographic mosaic of coevolution pronounced on the pollinator moths because adult beetles championed by Thompson (2005) suggests much of the inadvertently feed on pollinator moth eggs that are laid just dynamics of specialization and coevolution occurs among below the style surface (Segraves, 2008). The beetles could populations within a species. Greya politella, another prodoxid potentially act as indirect mutualists of the plants by limiting moth, is a pollinating seed parasite of prairie stars, Lithophragma the number of moth eggs and reducing the number of parviflorum, in the Inland Northwest of the western United seeds eaten. States. Depending on the population, the interaction can be Mutualisms can also attract a large number of other species antagonistic or mutualistic, yet be a stable coevolutionary that can exploit the resources produced. This is particularly hotspot (Thompson and Cunningham, 2002). prominent in the mutualism between figs and their pollinating Although specialization and coevolution are integral parts wasps. The fig is in essence an inflorescence that has been of mutualism, there are also many mutualisms in which mu- turned inside out and is pollinated by specialist agaonid wasps tualists are generalists and coevolutionary selection is likely that must crawl through a narrow channel to reach the minute weak (Waser et al., 1996). Many pollination and fruit dispersal flowers within the figinflorescence (Weiblen, 2002). As with mutualisms involve plants that attract a wide variety of pol- yucca moths, the female wasp lays eggs into the flowers and linators or dispersers. For example, saw palmetto populations then active pollinates each flower. The developing fig contains that occur along the Lake Wales ridge in Florida attract hun- both mature seeds and pollinator larvae that can be used as dreds of different species of floral visitors, many of which also resources by other species (Herre et al., 2008). Indeed, in some carry pollen (Deyrup and Deyrup, 2012). A similar pattern has localities in Australia, there are at least 12 other closely and also been found in the mutualism between ectomycorrhizal distantly related wasp species that come to figs to attack the fungi and trees in which fungal hyphal networks can involve seeds, attack the wasp larvae, or a combination of both (Segar many fungal species that connect to many different tree species et al., 2014). The presence of these additional community (Courty et al., 2010). A major approach to studying special- members might be one reason that female pollinator wasps ization and generalism in mutualism has been through only lay eggs in certain flowers within the fig(Al-Beidh et al., examination of mutualistic species interaction networks. These 2012). studies describe the patterns of connectedness among mutu- Addressing the role of additional community members on alists within a community (Bascompte and Jordano, 2013). mutualism is a daunting task given that there are many dif- Interestingly, a repeated pattern of connectedness is found in ferent species that can potentially influence a mutualism. This many mutualistic communities – networks involving inter- work becomes further complicated by the fact that the effects actions of mutualists are nested and asymmetric in the sense of different species can be nonadditive and may prevent us that there are generalist mutualist species that interact with a from making predictions. In many cases, a single species can subset of specialist mutualist species (Bascompte and Jordano, have both direct effects and indirect effects, and in other in- 2006). What remains to be tested is why such patterns of stances, the effect of one species might only be strong when in nestedness are prevalent, and why is it that some mutualists the presence of additional species. For example, in the defen- are specialists whereas others are generalists? sive mutualism between ants and plants, ants can be very 92 Mutualism, the Evolutionary Ecology of beneficial by protecting plants from herbivores. Unintention- Arditti, J., Elliott, J., Kitching, I.J., Wasserthal, L.T., 2012. ‘Good heavens ally, however, ants also deter pollinators from visiting the what insect can suck it’ − Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta. Botanical Journal of the Linnean Society 169, plants. Thus, when herbivores are rare, ant protection may – fi fi 403 432. shift from being very bene cial to less bene cial or even Bascompte, J., Jordano, P., 2006. The structure of plant−animal mutualistic harmful to plants (Ohm and Miller, 2014). Many more studies networks. In: Pascual, M., Dunne, J. (Eds.), Ecological Networks. Oxford: Oxford are needed to examine the role of local community members University Press, pp. 143–159. on the dynamics of mutualism. Only then can we begin to Bascompte, J., Jordano, P., 2013. Mutualistic Networks. Princeton, NJ: Princeton University Press. understand and predict how different types of community Bronstein, J.L., 1994. Conditional outcomes in mutualistic interactions. Trends in members may change the ecology and evolution of a focal Ecology & Evolution 9, 214–217. mutualism. Bronstein, J.L., 2001. The exploitation of mutualisms. Ecology Letters 4, 277–287. Bronstein, J.L., Alarcon, R., Geber, M., 2006. The evolution of plant-insect mutualisms. New Phytologist 172, 412–428. Bull, J.J., Harcombe, W.R., 2009. Population dynamics constrain the cooperative Synthesis evolution of cross-feeding. PLoS ONE 4. doi:10.1371/journal.pone.0004115. Bull, J.J., Rice, W.R., 1991. Distinguishing mechanisms for the evolution of co- – Mutualism has always attracted considerable attention because operation. Journal of Theoretical Biology 149, 63 74. Bshary, R., Schaffer, D., 2002. Choosy reef fish select cleaner fish that provide of the idea that species may help one another acquire resources high-quality service. Animal Behaviour 63, 557–564. or services. This is in part due to the fact that humans are Courty, P.-E., Buée, M., Diedhiou, A.G., et al., 2010. The role of ectomycorrhizal highly cooperative in our day-to-day activities. Research on communities in forest ecosystem processes: New perspectives and emerging mutualism, however, is demonstrating that natural selection concepts. Soil Biology and Biochemistry 42, 679–698. will always operate to increase the fitness of an organism. In Davis, D.R., 1967. A revision of the moths of the subfamily prodoxinae (Lepidoptera: Incurvariidae). United States National Museum Bulletin 255, 1–170. terms of thinking about mutualism, this means that species Deyrup, M., Deyrup, L., 2012. Diversity of insects visiting flowers of saw palmetto will continue to interact with their partner species as long as (Arecaceae). Florida Entomologist 95, 711–730. there is a net fitness benefit. To achieve this, there will be Frederickson, M.E., 2013. Rethinking mutualism stability: Cheaters and the evolution – evolution to decrease the costs of reciprocating and to increase of sanctions. Quarterly Review of Biology 88, 269 295. Goheen, J.R., Palmer, T.M., 2010. Defensive plant-ants stabilize megaherbivore- exploitation. Because of this underlying tension, mutualism is driven landscape change in an african savanna. Current Biology: CB 20, a highly dynamic interaction in which there is likely to be 1768–1772. continual evolution and coevolution among partner species. Grimaldi, D., 1999. The co-radiations of pollinating insects and angiosperms in the Sometimes this may lead to extreme specialization, but other cretaceous. Annals of the Missouri Botanical Garden 86, 373–406. fi times it might involve a suite of partner species. Adding to this Herre, E.A., Jandér, K.C., Machado, C.A., 2008. Evolutionary ecology of gs and their associates: Recent progress and outstanding puzzles. Annual Review of dynamism is the fact that other community members may Ecology, Evolution, and Systematics 39, 439–458. directly exploit resources or services provided by mutualists, Irwin, R.E., Brody, A.K., 1998. Nectar robbing in ipomopsis aggregata: Effects on thus adding to the costs of mutualism. What is perhaps most pollinator behavior and plant fitness. Oecologia 116, 519–527. fl fl astonishing is that mutualism has persisted since life began Marr, D.L., Pellmyr, O., 2003. Effect of pollinator-in icted ovule damage on oral abscission in the yucca-yucca moth mutualism: The role of mechanical and and continues to be an important interaction for generating chemical factors. Oecologia 136, 236–243. and maintaining biodiversity. Mee, M.T., Collins, J.J., Church, G.M., Wang, H.H., 2014. Syntrophic exchange in synthetic microbial communities. Proceedings of the National Academy of Science of the United States of America 111, 2149–2156. Ohm, J.R., Miller, T.E.X., 2014. Balancing anti-herbivore benefits and anti-pollinator – See also: Coevolution, Introduction to. Commensalism, costs of defensive mutualists. Ecology 95, 2924 2935. Pellmyr, O., 1999. Systematic revision of the yucca moths in Tegeticula yuccasella Amensalism, and Synnecrosis. Geographic Mosaic of Coevolution. complex (lepidoptera: Prodoxidae) north of Mexico. Systematic Entomology 24, Microbiome. Mycorrhizal Fungi, Evolution and Diversification of. 243–271. Plant–Pollinator Interactions and Flower Diversification. Predation Pellmyr, O., Balcázar-Lara, M., Althoff, D.M., Segraves, K.A., Leebens-Mack, J., and Parasitism. Symbiosis, Introduction to 2006. Phylogeny and life history evolution of Prodoxus yucca moths (lepidoptera: Prodoxidae). Systematic Entomology 31, 1–20. Pellmyr, O., Huth, C.J., 1994. Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372, 257–260. Powell, J., 1992. Interrelationships of yuccas and yucca moths. Trends in Ecology & Evolution 7, 10–15. References Rentsch, J.D., Leebens-Mack, J., 2014. Yucca aloifolia (Asparagaceae) opts out of an obligate pollination mutualism. American Journal of Botany 101, 2062–2067. Afkhami, M.E., Mcintyre, P.J., Strauss, S.Y., 2014. Mutualist-mediated effects on Sachs, J.L., Simms, E.L., 2006. Pathways to mutualism breakdown. Trends in species' range limits across large geographic scales. Ecology Letters 17, Ecology & Evolution 21, 585–592. 1265–1273. Sachs, J.L., Skophammer, R.G., Bansal, N., Stajich, J.E., 2014. Evolutionary origins Al-Beidh, S., Dunn, D.W., Power, S.A., Cook, J.M., 2012. Parasites and mutualism and diversification of proteobacterial mutualists. Proceedings of the Royal Society function: Measuring enemy-free space in a fig-pollinator symbiosis. Oikos 121, of London − Biological Sciences 281, 20132146. 1833–1839. Segar, S.T., Dunn, D.W., Darwell, C.T., Cook, J.M., 2014. How to be a fig wasp, Althoff, D., Segraves, K., Sparks, J., 2004. Characterizing the interaction between the down under: The diversity and structure of an australian fig wasp community. bogus yucca moth and yuccas: Do bogus yucca moths impact yucca Acta Oecologica-International Journal of Ecology 57, 17–27. reproductive success? Oecologia 140, 321–327. Segraves, K.A., 2008. Florivores limit cost of mutualism in the yucca−yucca moth Althoff, D.M., Xiao, W., Sumoski, S., Segraves, K.A., 2013. Florivore impacts on association. Ecology 89, 3215–3221. plant reproductive success and pollinator mortality in an obligate pollination Stanton, M.L., 2003. Interacting guilds: Moving beyond the pairwise perspective on mutualism. Oecologia 173, 1345–1354. mutualisms. American Naturalist 162, S10–S23. Anderson, B., Johnson, S.D., 2007. The geographical mosaic of coevolution in a Thompson, J.N., 1994. The Coevolutionary Process. Chicago, IL: University of plant-pollinator mutualism. Evolution 62 (1), 220–225. Chicago Press. Mutualism, the Evolutionary Ecology of 93

Thompson, J.N., 2005. The Geographic Mosaic of Coevolution. Chicago, IL: Weiblen, G.D., 2002. How to be a fig wasp. Annual Review of Entomology 47, University of Chicago. 299–330. Thompson, J.N., Cunningham, B.M., 2002. Geographic structure and dynamics of Weyl, E.G., Frederickson, M.E., Yu, D.W., Pierce, N.E., 2010. Economic contract coevolutionary selection. Nature 417, 735–738. theory tests models of mutualism. Proceedings of the National Academy of Van Beneden, P.J., 1873. Un mot sur la vie sociale des animaux inferieurs, série 2. Science of the United States of America 107, 15712–15716. Bulletin de l' Academie Royale de Belgique 36, 779–796. Yu, D.W., 2001. Parasites of mutualism. Biological Journal of the Linnean Society Waser, N.M., Chittka, L., Price, M.V., Williams, N.M., Ollerton, J., 1996. Generalization 72, 529–546. in pollination systems, and why it matters. Ecology 77, 1043–1060. Recombination and Molecular Evolution AJ Betancourt, Vetmeduni Vienna, Vienna, Austria M Hartfield, University of Toronto, ON, Canada r 2016 Elsevier Inc. All rights reserved.

Glossary Fitness Broadly, the ability of an individual to reproduce Adaptation The process of increasing in frequency a trait and leave descendants. that is beneficial under natural selection. Hitchhiking Where linked alleles (neutral or deleterious) Allele A gene type that is present at a locus. fix with an adaptive allele. Anisogamy The situation where male and female gametes Interference When selection acts on mutations in a non- are highly dimorphic; usually the male produces smaller independent manner (e.g., a deleterious allele hitchhikes to gametes. Isogamous species are where males and females fixation with an adaptive mutant). have similar-sized gametes. Linkage disequilibrium Nonrandom association of Background selection The loss of variation in the genome mutations in the genome. through purging deleterious mutation. Mutation A change made to the molecular sequence of a

Effective population size, Ne Aquantityusedtodescribe genome. the genetic diversity present in a population; the principle Recombination Reciprocal exchange of genetic material.

being that an idealized population of size Ne would harbor the Segregation When two gene copies are separated and are same level of diversity, if all mutations acted independently. passed at random during sexual reproduction. Epistasis The effect where a collection of loci exhibit different fitness, compared to cases where each mutation acts independently.

Introduction John Maynard Smith pointed out (Maynard Smith, 1978), asexual reproduction should have a twofold advantage, all else Many organisms reproduce sexually – 99.9% of animal spe- being equal. That is, asexual females will reproduce at twice cies, for instance (Vrijenhoek, 1998) – but the evolutionary the rate of sexual ones, quickly outcompeting them, so that a reason for the widespread prevalence of sex is not immediately mutation causing clonal reproduction in an anisogamous obvious. Sexual reproduction comes at a heavy price: mates species is expected to quickly take over (Figure 1). must be found, fought for, and won; sexually transmitted Nevertheless, sex is pervasive in many taxa. In fact, phylo- diseases braved; and, after all these trials, sexually-produced genetic analyses (Bell, 1982) show that sexual species tend to offspring only carry half the genes of the parent. In fact, as occur deeper in phylogenetic trees than asexual ones,

Sexuals Asexuals Males Females Females

Figure 1 A cartoon describing Maynard Smith’s ‘twofold cos of sex’ argument. The sexual population, on the left, requires a male and a female pairing to reproduce; if one son and daughter are born every generation, the population is maintained at the same size. Asexual females, on the right, can produce two clonal offspring without needing a male partner. Adapted from Hartfield, M., Keightley, P.D., 2012. Current hypotheses for the evolution of sex and recombination. Integrative Zoology 7, 192–209.

Encyclopedia of Evolutionary Biology, Volume 3 doi:10.1016/B978-0-12-800049-6.00177-3 411 412 Recombination and Molecular Evolution suggesting that only sexual species persist through time. For Recombination and Adaptation example, within the species Daphnia pulex, which has both sexual and asexual forms, the asexual lineages appear to be Theoretical Background short-lived (Tucker et al., 2013). What, then, might account for Any selected allele, whether deleterious or beneficial, must the apparent advantage of sexual lineages? One possibility is begin as a mutation, either as a single or multiple copies. Each that there are immediate advantages to sexual reproduction; copy of the allele will arise on some genetic background, for example, receiving care from two parents might improve usually one randomly drawn from the population. Without the survival of offspring. That is, while the twofold cost of sex recombination, the fate of the selected allele is strongly af- is useful as a thought experiment, it might rarely be realized in fected by whichever genetic background it arises on. For ex- nature, as reproductive rates alone are not always the principal ample, a beneficial allele unlucky enough to arise on an unfit determinant of evolutionary fitness. However, this rationale genetic background may be lost, driven out of the population depends on details of the life history of each species, and is along with the deleterious alleles it is linked to. When the fates therefore unsatisfying as a general explanation for the preva- of selected alleles are non-independent, they are said to lence of sex. ‘interfere’ with one another. Felsenstein (1974), in an engaging Instead, it is generally thought that sexual lineages have a review of the topic, termed this phenomenon 'Hill–Robertson long-term fitness advantage over asexual lineages. Sexual species interference,' after the seminal investigation into selection, are expected to adapt faster to changing environments, and to linkage, and drift interactions by Hill and Robertson (1966). better maintain fitness in constant environments, compared to There are several flavors of Hill–Robertson interference, asexual organisms. The reason is that sex shuffles genomes, but all ultimately attribute the evolutionary advantage of re- making new combinations of genotypes available for selection combination to its ability to uncouple selected alleles from to act on. Mechanistically, this shuffling comes in two flavors: their genetic backgrounds, so selection can act on them segregation and recombination between loci (Figure 2). Both independently. are expected to promote the spread of beneficial mutations and the purging of deleterious ones. Without segregation, for ex- 1. Fisher–Muller interference. Fisher (1930) and Muller ample, the descendants of a heterozygous individual will re- (1932) pointed out how asexual populations suffer from main heterozygous ad infinitum, or at least until a second interference between beneficial mutations. That is, in a mutation occurs at the same locus. A single beneficial mutation non-recombining population, in order for two (or more) in such a population can increase from low frequency to 50%, beneficial mutations to fix at the same time, they must but then faces a barrier to fixation. With segregation, there is no occur in the same genetic background. This composition is such barrier; homozygous individuals are easily generated from unlikely, unless the first beneficial mutation to occur has heterozygous ones, and the beneficial mutation can fully spread already reached a high frequency. With recombination, (Kirkpatrick and Jenkins, 1989). two beneficial mutations can occur on different back- The overwhelming body of research, though, is directed grounds, recombine onto the same genome, and sweep to toward the evolutionary benefits of genetic recombination. As fixation together (Figure 3). Thus, fixing two mutations we will discuss below, the implications of recombination have takes roughly half the time that it does in an asexual been spelled out in a large body of theory, some of which has population (Christiansen et al., 1998), unless mutation been tested with molecular data. rates are high enough to create double mutants without

Segregation Recombination

A B C D

A C B D

Figure 2 Segregation and recombination during sex. Segregation shuffles the manner in which gene copies (denoted here A–D and labeled with different colors) are organized within genomes. Recombination exchanges material between genomes. Recombination and Molecular Evolution 413

Asexual population aaBB

Frequency of genotype AAbb ab ABAB in space

aBaB

(a) Generations

Sexual population

Frequency of genotype AbAb in space ab ABAB aBaB

(b) Generations Figure 3 Fisher–Muller argument for the evolution of sex. In asexuals (top), beneficial mutations have to arise and fix in sequence due to competition between them. In sexuals (bottom), however, recombination can form the optimal AB genotype much more rapidly. Adapted from Muller, H.J., 1932. Some genetic aspects of sex. American Naturalist 66, 118–138.

recombination (Kim and Orr, 2005). When applied to force, causing genomic degradation (Charlesworth and microbes, Fisher–Muller interference is sometimes called Charlesworth, 2000). ‘clonal interference’ (Gerrish and Lenski, 1998), which can 3. Ruby-in-the-rubbish interference. Ruby-in-the-rubbish be tested experimentally (e.g., Lang et al. (2013)). interference (Peck, 1994) describes the loss of beneficial 2. Muller’s ratchet. Muller’s(Muller, 1964) ratchet does not mutations that happen to arise on unfit backgrounds. The describe a failure to adapt to a changing environment, but original ruby-in-the-rubbish model considers adaptation instead a failure to maintain fitness even in a constant in an asexual population, where the beneficial mutations environment. In any population, particularly a small one, are not strong enough to overcome the effect of linked it is always possible to lose the fittest current genotype by deleterious mutations. In this case, the only beneficial chance. One way to model this phenomena is to consider mutations with any chance of not going extinct must arise deleterious mutations to be Poisson distributed over on deleterious-mutation-free genomes. In sexual popu- chromosomes À essentially, distributed in the same way lations, recombination can free the beneficial mutation beans dropped onto a chessboard would be randomly from its loaded genetic background, improving its pro- spread over the squares. As Haigh (1978) showed, the spects for success. Cases in which the beneficial mutations mean number of mutations would be the ratio of the are strongly selected for, and therefore override linked genomic mutation rate (U) to the average selection co- deleterious mutations, are more complex. If there are

efficient acting against these mutations (sd). The fraction of many deleterious mutations, adaptive alleles can still be deleterious-mutation-free genomes is then just the size of lost in asexual populations if mutation rates are high

the zero class for the Poisson distribution, exp(-U/sd). (Johnson and Barton, 2002). With pairs of advantageous– Thus, if the fraction of individuals carrying no deleterious deleterious mutations, sex can prevent the fixation of mutations is expected to be one in a thousand, a popu- deleterious alleles. The benefit to recombination is greatest lation with a census size in the hundreds may not contain if deleterious mutations have slightly lower selection co- even one individual without deleterious mutations. In an efficients than their beneficial drivers (Hartfield and Otto, asexual population, with no back mutation, there is also 2011). However, the case with many deleterious mu- no way to regenerate a mutation-free genome À the name tations affecting adaptive alleles in sexual populations has ‘Muller’s ratchet’ comes from this irreversibility, as ratchets not yet been fully solved. are wrenches that turn only one direction. Recombination, however, can reverse the process: as long as no particular In each of these cases, recombination counteracts inter- deleterious mutation fixes, two genomes can recombine to ference by offering new allele combinations for selection to act form a reconstituted mutation-free genome. on. This effect is only useful, though, when the fittest alleles As the arguments above suggest, Muller’s ratchet is most are not already found together; otherwise, recombination important in small populations, with high genomic mu- breaks apart optimal genotypes. In technical terms, re- tation rates (due to either high overall mutation rates, and/ combination only provides a benefit if there is negative linkage or long genomes), or with weak selection (Felsenstein, between beneficial mutations – when genomes more often 1974). Without these factors, the ratchet acts so slowly have a mixture of beneficial and deleterious alleles at different as to be unimportant; otherwise it can be a powerful loci, rather than possess only beneficial or only deleterious 414 Recombination and Molecular Evolution alleles. What, then, should give rise to these kinds of non- in humans (Wilson Sayres et al., 2014), mice (Soh et al., 2014), random associations? One answer is epistasis, where indi- and plants (Hough et al., 2014); see Bachtrog (2013) for a viduals carrying multiple mutations have better or worse recent review. fitness than expected based on the selective coefficients of the Other studies looking for an evolutionary advantage of single mutations. However, only specific kinds of epistasis recombination have been done within chromosomes, com- promote increased recombination (see Kondrashov (1988) paring low to high recombination regions. In Drosophila mel- and Kouyos et al. (2007)). A general explanation may simply anogaster, for example, there are long regions exhibiting very be that population sizes are limited. As Fisher (1930) pointed low recombination rates. Molecular evidence suggests that out, in any finite population, all possible combinations of these regions show fewer substitutions of adaptive alleles and alleles never occur, so there will always be nonrandom asso- more substitutions of deleterious alleles, compared to regions ciations between alleles. In cases where beneficial mutations of average recombination (Betancourt and Presgraves, 2002; are coupled, selection will quickly fix these genotypes (and, Haddrill et al., 2007; Mackay et al., 2012). Gossmann et al. conversely, rapidly purge genotypes where deleterious mu- (2014) also found such a result in birds, by comparing tations are coupled). The upshot is that the genotypes con- chromosomes with different average recombination rates. taining a mixture of beneficial and deleterious mutations Humans, in contrast, do not show a strong pattern of this type would, on average, remain segregating for the longest amount (Bullaughey et al., 2008), possibly due a low rate of adaptive of time. Over time, then, most linkage disequilibrium between protein evolution in our own species (Eyre-Walker and beneficial mutations is negative, of just the sort to promote an Keightley, 2009). advantage of recombination. Barton and Otto (2005) solidi- fied this logic and showed how associations created in this manner select for increased recombination rates. Recombination and Neutral Variation

Empirical Evidence for an Advantage of Recombination Even in sexual organisms, the amount of recombination can vary, for example, across sexes and individuals, and even If there is an advantage of recombination in aiding adaptation, across the genome. Studies of how evolutionary rates differ can we see it in molecular population genetic data? Some of due to this variation have yielded fascinating insights into the the earliest answers to this question come from sex chromo- effects of selection interference. D. melanogaster is an organism somes, which have evolved independently many times from that shows a large amount of variation in recombination rates autosomes. X and Y chromosomes proceed to diverge when across its genome. In the early 1990s, Begun and Aquadro recombination between them stops; as the Y only occurs while (1992) used this fact to show that, compared to highly re- paired with the X, it can no longer recombine at all. What combination regions, low recombination regions had very happens to this non-recombining chromosome? The long- little genetic diversity – in these regions, individual sequences term outcome can be seen on the Drosophila Y, for example. In of the same gene, which in D. melanogaster differ from each terms of DNA content, this chromosome is huge – roughly other at 1–2% of silent sites, showed only a small fraction of twice the size of the X – but it harbors only a handful of genes, the normal level of variation. They invoked an explanation for compared to thousands on the X. Initially, these chromosomes which the theory had been worked out 20 years before: were identical, but the Y has lost most of its genes, and gained hitchhiking of neutral mutations (Maynard Smith and Haigh, a large amount of ‘junk DNA.’ By studying young Y chromo- 1974), based on Hill–Robertson interference caused by bene- somes, we can watch this process in action. For example, there ficial mutations. Briefly, hitchhiking argues that if selection is a very young Y chromosome in Drosophila miranda, which fixes a single copy of a beneficial allele, it necessarily also fixes still retains many of its genes. Compared to their homologous any neutral variants that arise on the same background on the X, however, these copies show less evidence of adap- (Figure 4). As a result, the nearby regions will be stripped of tation (Bachtrog and Charlesworth, 2000) as predicted by the neutral variation. Recombination, however, allows the selected theories outlined above. Similar surveys have been performed allele to move to other genetic backgrounds, and be linked to

Hitchhiking Background selection

Before Before selection selection

After After selection selection

Figure 4 How selective effects reduce genetic variance. Hitchhiking (left) occurs when an adaptive allele, shown in red, spreads to all individuals in the population. Linked neutral mutations (blue dots) are driven with it to fixation as well, unifying the genetic signal around the adaptation. Background selection (right) occurs when deleterious mutations, the gray dots, are lost by selection, and are replaced by other neutral genotyped (after selection, the second genotype is replaced by the third, and the fifth by the fourth). Recombination and Molecular Evolution 415 other neutral alleles; thus, the extent of the region affected by (Marais et al., 2001; Haddrill et al., 2007; Campos et al., 2014). hitchhiking depends on the recombination rate. The reason is likely historical: weakly selected sites will take a More formally, we can see why recombination should af- long time to reach their equilibrium level of adaptation, while fect neutral sequence diversity if we first understand what af- most reduced recombination regions in D. melanogaster seem fects it, namely, mutation rate (u), and the number of to have only recently suffered from a reduction in recombin- ancestors contributing genetic material to a population, ation rate (Campos et al., 2014). Further, with whole-genome quantified as effective population size (Ne). Diversity increases polymorphism data, we have been able to refine our picture of as mutation rate increases, because, as more mutations are the local effect of selection on linked neutral sites. In the im- introduced into a population, more sites can contain differ- mediate vicinity of putatively adaptive substitutions, there is a ences. Diversity also increases as Ne increases – if the number dip in average neutral diversity, just as expected under of genetic ancestors is small, individuals will be closely related, hitchhiking (Sattath et al., 2011), though not in humans and therefore genetically similar to one another. Begun and (Hernandez et al., 2011). In our own species, the role of Aquadro were able to eliminate an effect of recombination on background selection is well-established; in fact, the effect of mutation rate, and therefore concluded that recombination linkage to selected sites has been quantified in a ‘background affects Ne. As diversity is measured across the genome of a selection map’ (McVicker et al., 2009). The contrast between single species of fly, it is unlikely that there are different Drosophila, which shows evidence consistent with adaptive numbers of actual ancestors contributing to different regions evolution, and humans, where deleterious mutations appear of the genome. Instead, it may be that the fixation of beneficial to play a bigger role, may be due to their contrasting effective mutations reduces the number of genetic ancestors for long population sizes. All else being equal, larger populations may regions in low recombination regions via the hitchhiking effect experience higher overall rates of adaptive substitutions: in (Figure 4). support of this, mice, which are mammals like humans but Hitchhiking, then, appears to explain the relationship be- have larger population sizes (Phifer-Rixey et al., 2012), show a tween diversity and recombination, which also implies that Drosophila-like pattern near substitutions (Halligan et al., adaptive evolution is frequent enough to change levels of 2013). neutral diversity. However, Charlesworth et al. (1993) almost immediately challenged this explanation, pointing out that hitchhiking is not the only possible cause for a relationship Conclusion between neutral diversity and recombination, recurrent dele- terious mutations is another. The reason is that deleterious Here, we have seen how recombination frees organisms to mutations also reduce the effective population size of linked adapt at multiple sites, allows them to preserve the integrity of regions: as they are removed from the population, so is any their genomes, and conserves genetic variation. With reduced neutral linked variation (Figure 4). Without recombination, sequencing costs, these questions can now be addressed in the only genomes that ultimately contribute ancestry to the new species and in new ways. Future results will refine our population are those deleterious-mutation-free genomes; that picture on how recombination shapes genomes, and hopefully is, the zero class of the Muller's ratchet model. With re- throw up unexpected outcomes, generating new avenues of combination, some of the genetic material that would have research. otherwise been lost can recombine onto mutation-free back- grounds. As a result, the effect of background selection, like that of hitchhiking, varies with the recombination rate. Trying See also: Effective Population Size. Recombination and Selection. to disentangle the two effects still motivates current research, Selective Sweeps. Sex, Evolution and Maintenance of since the two phenomena can be difficult to tease apart (Cutter and Payseur, 2013). Begun and Aquadro’s observations were based on a limited References amount of data (appropriate for the time), so it is worth fi asking how their ndings have held up. For Drosophila, the Bachtrog, D., 2013. Y-chromosome evolution: Emerging insights into processes of answer is quite well, as shown using whole-genome poly- Y-chromosome degeneration. Nature Reviews Genetics 14, 113–124. morphism datasets (Mackay et al., 2012). Besides Drosophila, Bachtrog, D., Charlesworth, B., 2000. Reduced levels of microsatellite variability on these effects have been examined in a broad range of taxa the neo-Y chromosome of Drosophila miranda. Current Biology 10, 1025–1031. (Cutter and Payseur, 2013); though the results are mixed, most Barton, N.H., Otto, S.P., 2005. Evolution of rRecombination due to random drift. other taxa show similar patterns to those in Drosophila, with Genetics 169, 2353–2370. recombination rate positively correlated with neutral genetic Begun, D.J., Aquadro, C.F., 1992. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520. diversity. The effect of recombination on Ne is also reflected in patterns seen for weakly selected alleles: alleles whose selec- Bell, G., 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. fi Berkeley: University of California Press. tion coef cients hover near the value of 1/Ne, rendering them Betancourt, A.J., Presgraves, D.C., 2002. Linkage limits the power of natural borderline neutral. A local reduction in Ne can push them selection in Drosophila. Proceedings of the National Academy of Sciences of the under this threshold, so that they act effectively neutrally. In United States of America 99, 13616–13620. Drosophila, sites evolving under weak selection do, in fact, Bullaughey, K., Przeworski, M., Coop, G., 2008. No effect of recombination on the efficacy of natural selection in primates. Genome Research 18, 544–554. show reduced adaptation in regions of very low recombin- Campos, J.L., Halligan, D.L., Haddrill, P.R., Charlesworth, B., 2014. The relation ation. However, this effect appears to be restricted to these between recombination rate and patterns of molecular evolution and variation in regions, rather than scaling with increased recombination rate Drosophila melanogaster. Molecular Biology & Evolution 31, 1010–1028. 416 Recombination and Molecular Evolution

Charlesworth, B., Charlesworth, D., 2000. The degeneration of Y chromosomes. Kirkpatrick, M., Jenkins, C.D., 1989. Genetic segregation and the maintenance of Philosophical Transactions of the Royal Society of London, B: Biological sexual reproduction. Nature 339, 300–301. Sciences 355, 1563–1572. Kondrashov, A.S., 1988. Deleterious mutations and the evolution of sexual Charlesworth, B., Morgan, M.T., Charlesworth, D., 1993. The effect of deleterious reproduction. Nature 336, 435–440. mutations on neutral molecular variation. Genetics 134, 1289–1303. Kouyos, R.D., Silander, O.K., Bonhoeffer, S., 2007. Epistasis between deleterious Christiansen, F.B., Otto, S.P., Bergman, A., Feldman, M.W., 1998. Waiting with and mutations and the evolution of recombination. Trends in Ecology & Evolution 22, without recombination: The time to production of a double mutant. Theoretical 308–315. Population Biology 53, 199–215. Lang, G.I., Rice, D.P., Hickman, M.J., et al., 2013. Pervasive genetic hitchhiking and Cutter, A.D., Payseur, B.A., 2013. Genomic signatures of selection at linked sites: clonal interference in forty evolving yeast populations. Nature 500, 571–574. Unifying the disparity among species. Nature Review Genetics 14, 262–274. Mackay, T.F.C., Richards, S., Stone, E.A., et al., 2012. The Drosophila melanogaster Eyre-Walker, A., Keightley, P.D., 2009. Estimating the rate of adaptive molecular Genetic Reference Panel. Nature 482, 173–178. evolution in the presence of slightly deleterious mutations and population size Marais, G., Mouchiroud, D., Duret, L., 2001. Does recombination improve selection change. Molecular Biology & Evolution 26, 2097–2108. on codon usage? Lessons from nematode and fly complete genomes. Felsenstein, J., 1974. The evolutionary advantage of recombination. Genetics 78, Proceedings of the National Academy of Sciences of the United States of 737–756. America 98, 5688–5692. Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford: The Clarendon Maynard Smith, J., 1978. The Evolution of Sex. Cambridge; New York: Cambridge Press. University Press. Gerrish, P., Lenski, R., 1998. The fate of competing beneficial mutations in an Maynard Smith, J., Haigh, J., 1974. The hitch-hiking effect of a favourable gene. asexual population. Genetica 102−103, 127–144. Genetics Research 23, 23–35. Gossmann, T.I., Santure, A.W., Sheldon, B.C., Slate, J., Zeng, K., 2014. Highly McVicker, G., Gordon, D., Davis, C., Green, P., 2009. Widespread genomic variable recombinational landscape modulates efficacy of natural selection in signatures of natural selection in hominid evolution. PLoS Genetics 5, e1000471. birds. Genome Biology & Evolution 6, 2061–2075. Muller, H.J., 1932. Some genetic aspects of sex. American Naturalist 66, 118–138. Haddrill, P., Halligan, D., Tomaras, D., Charlesworth, B., 2007. Reduced efficacy of Muller, H.J., 1964. The relation of recombination to mutational advance. Mutation selection in regions of the Drosophila genome that lack crossing over. Genome Research/Fundamental and Molecular Mechanisms of Mutagenesis 1, Biology 8, R18. 2–9. Haigh, J., 1978. The accumulation of deleterious genes in a population − Muller's Peck, J.R., 1994. A ruby in the rubbish: Beneficial mutations, deleterious mutations Ratchet. Theoretical Population Biology 14, 251–267. and the evolution of sex. Genetics 137, 597–606. Halligan, D.L., Kousathanas, A., Ness, R.W., et al., 2013. Contributions of protein- Phifer-Rixey, M., Bonhomme, F., Boursot, P., et al., 2012. Adaptive evolution and coding and regulatory change to adaptive molecular evolution in murid rodents. effective population size in wild house mice. Molecular Biology & Evolution 29, PLoS Genetics 9, e1003995. 2949–2955. Hartfield, M., Otto, S.P., 2011. Recombination and hitchhiking of deleterious alleles. Sattath, S., Elyashiv, E., Kolodny, O., Rinott, Y., Sella, G., 2011. Pervasive adaptive Evolution 65, 2421–2434. protein evolution apparent in diversity patterns around amino acid substitutions Hernandez, R.D., Kelley, J.L., Elyashiv, E., et al., 2011. Classic selective sweeps in Drosophila simulans. PLoS Genetics 7, e1001302. were rare in recent human evolution. Science 331, 920–924. Soh, Y.Q.S., Alföldi, J., Pyntikova, T., et al., 2014. Sequencing the mouse Y Hill, W.G., Robertson, A., 1966. The effect of linkage on limits to artificial selection. chromosome reveals convergent gene acquisition and amplification on both sex Genetic Research 8, 269–294. chromosomes. Cell 159, 800–813. Hough, J., Hollister, J.D., Wang, W., Barrett, S.C.H., Wright, S.I., 2014. Genetic Tucker, A.E., Ackerman, M.S., Eads, B.D., Xu, S., Lynch, M., 2013. Population- degeneration of old and young Y chromosomes in the flowering plant Rumex genomic insights into the evolutionary origin and fate of obligately asexual hastatulus. Proceedings of the National Academy of Sciences of the United Daphnia pulex. Proceedings of the National Academy of Sciences of the United States of America 111, 7713–7718. States of America 110, 15740–15745. Johnson, T., Barton, N.H., 2002. The effect of deleterious alleles on adaptation in Vrijenhoek, R.C., 1998. Animal clones and diversity. BioScience 48, 617–628. asexual populations. Genetics 162, 395–411. Wilson Sayres, M.A., Lohmueller, K.E., Nielsen, R., 2014. Natural selection reduced Kim, Y., Orr, H.A., 2005. Adaptation in sexuals vs. asexuals: Clonal interference and diversity on human Y chromosomes. PLoS Genetics 10, e1004064. the Fisher−Muller model. Genetics 171, 1377–1386. Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth MA Schenkel and LW Beukeboom, University of Groningen, Groningen, The Netherlands r 2016 Elsevier Inc. All rights reserved.

Glossary Recombination Exchange of genetic content between Androdioecy Reproductive system in which individuals chromosomes during mitosis or meiosis. are either male or hermaphroditic. Sex chromosomes The chromosome pair on which the Dioecy Reproductive system in which individuals are master sex determination gene is located, leading to these either male or female. chromosomes being transmitted differently through both Gynodioecy Reproductive system in which individuals are sexes. either female or hermaphroditic. Sex determination Process directing development into a Heterogamety Production of gametes with different sexually functional individual. sex chromosomes (e.g., X- and Y-carrying sperm in Sexual conflict Differences between sexes in optimal humans). fitness strategies. Homogamety Production of gametes with similar Sexually antagonistic genes Genes that are under sex chromosomes (e.g., X-carrying egg cells in humans). different selective forces between males and females.

Introduction limited to males. Over time, the minor sex chromosome re- verses to a mostly haploid and clonal lifestyle and adapts to its Eukaryotic genomes typically consist of several chromosomes sex-limited role (Rice, 1988; Bachtrog, 2013). However, the that contain an individual’s genetic information. Sex lack of recombination leads to the degeneration of the chromosomes carry the master sex-determining genes, causing chromosome, as mutations accumulate and genes are lost. In them to be transmitted differently through the sexes. Con- humans, the Y chromosome is much smaller than the X sequently, they are subject to different selection forces com- chromosome, and carries only few functional genes. Due to pared to their autosomal counterparts (see Table 1) and their specific genomic niche and inheritance pattern, sex follow an evolutionary trajectory that deviates from the rest of chromosomes can play important roles in processes such as the genome (Rice, 1988). It is generally accepted that sex speciation, sexual selection, and genomic conflict (e.g., Werren chromosomes originate from autosomes by acquiring a sex and Beukeboom, 1998; Kirkpatrick and Hall, 2004; Presgraves, determination function. 2008; Demuth et al., 2014). In diploid heterogametic systems, which are found in most Sex chromosomes are found in a wide variety of organisms, animals and some plants, one sex chromosome, referred to as ranging from fungi to plants and animals. They are associated the major sex chromosome, is transmitted through both sexes. with diverse sex determination mechanisms, though several The other sex chromosome, referred to as the minor sex sex determination mechanisms without sex chromosomes also chromosome in the heterogametic sex, is sex-limited in its exist (reviewed in Beukeboom and Perrin, 2014; Bachtrog inheritance. For example, in humans the X chromosome is et al., 2014). Systems with sex chromosomes can be classified transmitted through both sexes, whereas the Y chromosome is in three distinct groups. First, in XY systems, which are found

Table 1 Features of sex chromosomes in comparison to autosomes. Sex chromosomes are responsible for sex determination in the haploid (U and V) or diploid (W, X, Y, and Z) phase of the life cycle and are transmitted through one or both the sexes. Recombination between different types of sex chromosomes is suppressed. Sex chromosomes have different effective population sizes compared to autosomes

Y/W Z/X U V Autosome

Phase in life cycle in diploid diploid haploid haploid not applicable which sex is determined Sex-specific yes, Y through no, but X twice as yes, through female yes, through male No inheritance males, W through often through gametophyte gametophyte females females, Z twice as often through males Recombination suppressed unsuppressed in the suppressed suppressed yes homogametic sex, suppressed in the heterogametic sex Effective population 1/4 3/4 1/2 1/2 1 size

72 Encyclopedia of Evolutionary Biology, Volume 4 doi:10.1016/B978-0-12-800049-6.00147-5 Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth 73 in most mammals and insects, sex is determined in the diploid Charlesworth and Charlesworth, 1978; Charlesworth, 2013 for phase of the life cycle. In these systems, males are the het- further details). erogametic sex. Second, ZW systems are similar to XY systems, Sex chromosomes may support different forms of sex de- but instead the female is the heterogametic sex. Organismal termination. One possibility is that they carry a dominant gene groups in which ZW systems are found include birds, butter- for maleness (Y) or femaleness (W), such as the mammalian flies, and moths. Third, in UV systems sex is determined in the SRY (Berta et al., 1990), DMY in fish (Matsuda et al., 2002), or haploid phase of the life cycle, with the U chromosome in M-factors in houseflies (reviewed in Dübendorfer et al., 2002). females and the V chromosome in males. UV systems are Another possibility is that sex chromosomes are being counted, found in, for example, fungi, algae, and mosses. Some orga- one sex having two copies and the other only one (X or Z). This nismal groups, such as fish and amphibians, are rather diverse is, for example, the case in Drosophila (reviewed in Cline, 1993; when it comes to sex chromosome systems. In such groups, see also Ericksson and Quintero, 2007), and may be rather some species have XY systems, whereas others have a ZW common given the frequency of XO and ZO systems in nature. system. In some cases, the Y or W chromosome is absent. Such Though the associated genetic mechanisms of sex de- systems are referred to as XO and ZO, meaning that the het- termination and the selective forces driving their evolution may erogametic sex produces one type of gamete with and one type differ substantially between species, clear similarities can be of gamete without the major sex chromosome. XO systems are distinguished in the evolution of proto-sex chromosomes (re- frequently found in insects such as beetles and grasshoppers; viewed in Bachtrog et al.,2014).Aftertheyhavebeenformed, ZO systems are less common. Finally, systems with multiple proto-sex chromosomes may undergo rapid evolution as a re- sex chromosomes are also known, but these are rare. sult of their different transmission through the sexes (Rice and The division in homo- and heterogametic sexes stems from Holland, 1997; Charlesworth, 2013), with the minor sex the fact that one sex carries two identical (homomorphic) sex chromosome becoming haploid and restricted to one sex. chromosomes that are inherited equally to sons and daugh- ters, whereas the other sex carries one sex chromosome that inherits to sons and one that inherits to daughters only. In Sexual Conflict and Sex Chromosomes male heterogametic systems, the male has one X and one Y chromosome, and the female two X chromosomes; the Y Males and females often experience different selective pressures. chromosome is male-determining. In female heterogametic Because sex chromosomes are transmitted differently through systems, the female carries one Z and one W chromosome, and the sexes, they are a potential hotspot for genes that are under the male two Z chromosomes; the W chromosome is female- different selective forces in males and females (Rice, 1984). A determining. As the sex-limited chromosomes are often dif- locus that is selected differently depending on its genetic ferent in size and genetic composition (heteromorphic), this is background experiences genetic conflict (Rice, 1987a; Werren called the heterogametic sex. and Beukeboom, 1998; Stewart et al.,2010). Selection on autosomes will be toward optima intermediate to those ex- perienced by both sexes, whereas for sex-linked genes selection Acquisition of a Sex-Determining Function will lead to the optimum experienced by the sex to which these genes are linked. Rice (1984, 1994, 1998) showed that exclusive Several phases can be distinguished in the evolution of sex transmission of a chromosome through one sex can lead to chromosomes. Sex chromosomes are formed when an auto- accumulation of alleles on that chromosome that are beneficial some gains a sex-determining function (Charlesworth et al., for that sex but detrimental for the other sex. Such genes that 2005; Pease and Hahn, 2012, but see Carvalho et al., 2009), experience differences in selection sign or strength between typically by acquiring genes causing carriers to develop into a sexes are referred to as sexually antagonistic (SA) genes. When specific sex. This can happen through translocation of existing linked to an SD gene, SA allele frequencies may shift between sex determination (SD) genes from other chromosomes, fu- the sexes, allowing for the resolution of genetic conflict (Rice, sion of an autosome with an existing sex chromosome, or 1987a). However, resolving genetic conflict between the sexes through de novo origin of an SD gene, such as the mammalian may not necessarily require translocation to the sex chromo- SRY (sex-determining region Y) gene which came into being by somes. Gene expression may already be dependent on sex mutation of the Sox3 gene in the ancestor of therians some 150 (Stewart et al.,2010), allowing for divergence of gene expression million years ago. Chromosomes that have recently gained and conflict resolution. The association between SD and SA a sex-determining function are referred to as proto-sex genes may be explained by an SD gene evolving near SA genes, chromosomes or neo-sex chromosomes. which may be favorable to the spread of the new proto-sex Hermaphrodites may give rise to separate sexes, thereby chromosome (Van Doorn and Kirkpatrick, 2010). However, producing proto-sex chromosomes (Charlesworth and Char- enrichment in SA genes on sex chromosomes relative to auto- lesworth, 1978; Charlesworth, 2013). In this scenario, a loss- somes suggests that these genes were translocated from other of-function or sterility mutation may cause hermaphroditic genomic regions to the sex chromosome (Mank, 2012). individuals to develop into one sex; a subsequent mutation in Though genetic conflict theory predicts that the X and Y the remaining hermaphrodites may then cause offspring to chromosomes become enriched for female- and male-bene- develop into the other sex. Such mutation may first lead to ficial genes respectively, this need not necessarily be true. A development of females (gynodioecy) or males (androdioecy) male-beneficial gene may spread when X-linked provided that depending on which sexual traits are affected by these loss-of- it is at least partially recessive (Rice, 1988; Graves, 2006). In function mutations, before complete dioecy is established (see males, such a gene may easily have its beneficial effect as it is 74 Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth hemizygous, whereas in females the deleterious effects may be Second, extensive methylation is known to inhibit re- sheltered by dominant alleles. Similarly, the X chromosome combination (Maloisel and Rossignol, 1998; Melamed-Bes- may be enriched for female-beneficial genes, though these are sudo and Levy, 2012). Increased methylation in the SDR of the only expected to spread easily when sufficiently dominant proto-sex chromosome may lead to reduced recombination (reviewed in Ellegren and Parsch, 2007). levels between SD and SA loci (Maloisel and Rossignol, 1998; Gorelick, 2003; Melamed-Bessudo and Levy, 2012). This is in accordance with findings that in some species, for example Suppression of Recombination sticklebacks, recombination between the sex chromosomes stopped in a very gradual fashion (Chibalina and Filatov, Why Does Suppression of Recombination Occur? 2011; Natri et al., 2013; Roesti et al., 2013). Third, sufficient levels of sequence divergence between The suppression of recombination along the minor sex homologues reduce recombination rates. Though sequence chromosome is a key step in sex chromosome evolution. It divergence appears unlikely to evolve between recombining fl prevents gene ow between the sex chromosomes and leads to chromosomes, such divergence can be accelerated by the non-recombining region becoming sex-limited and thus chromosomal inversions (Andolfatto et al., 2001). Inversions effectively haploid (Charlesworth, 1978). This causes progressive have been proposed as an explanation for evolutionary strata divergence between the sex chromosomes and leads to the de- on sex chromosomes in various species (e.g., Lahn and Page, generation of the minor sex chromosome (see also below). 1999; Wright et al., 2014). Late-stage minor sex chromosomes typically no longer re- Extensive methylation and inversions can cause local sup- combine along the majority of its length, except for in a small pression of recombination and can be regarded as specialized terminal region known as the pseudoautosomal region (PAR, forms of the suppressor-gene model (Nei, 1969). These mu- reviewed in Otto et al., 2011). The PAR may be involved in tations may spread provided they are linked to a beneficial obligate recombination during meiosis; however, its absence combination of genes. Theoretical studies have shown that this in some species shows this is not a universal requirement. The is indeed true for inversions (Kirkpatrick, 2010), but similar discovery of several evolutionary strata on therian X chromo- results are expected in case of extensive methylation. somes (Lahn and Page, 1999; Nicolas et al., 2005; Roesti et al., 2013), as well as differing degrees of divergence between X- and Y-linked genes (Chibalina and Filatov, 2011; Zhou and Bachtrog, 2012b; Natri et al., 2013) suggest that recombination Sex Chromosome Degeneration does not halt abruptly, but rather spreads along the chromo- Recombination and Selection some in a stepwise or gradual fashion. Suppression of re- combination will start at the sex-determining region (SDR) for Though suppressed recombination may allow for faithful two possible reasons. First, crossovers in the SDR may be se- transmission of co-adapted gene complexes, it also induces the lected against because it results in improper sex determination. degeneration of the minor sex chromosome. Various models Second, breaking up the association between SD and SA genes describe how suppressed recombination induces degeneration (Rice, 1987a) leads to SA genes being passed on to offspring (Figure 1). These can be classified according to two effects of that will develop into the sex in which they have a deleterious recombination: (1) the creation of novel genotypic combin- effect, which will be selected against. Tight linkage between SD ations and (2) the ability to select on loci separately. Genome- fi and SA genes allows for stronger sex-speci c adaptation and wide effects include Muller’s ratchet, a process that leads to thus suppressed recombination may be favorable (Muller, the random loss of mutation-free chromosomes, and Hill– 1964; Nei, 1969). As more and more SA genes accumulate on Robertson interference, the inability to combine beneficial the sex chromosomes, this suppression of recombination is mutations if these arise on separate chromosomes. Locus- believed to spread outward, until the full chromosome experi- specific processes refer to the interdependence between fitness ences suppressed recombination. It should be noted that this effects of loci and their genetic background. theoretical model of SD and SA gene interaction is broadly Muller’s ratchet is considered to be the main cause of accepted but that the experimental support is still weak. mutation accumulation (Muller, 1918; Muller, 1964). It as- sumes that mutations occur readily, that these mutations are How Is Recombination Suppressed? typically near-neutral and thus do not suffer from selection until the mutational load transgresses a certain threshold (see The proximate causes of recombination suppression are not also Rice, 1996). Recombination may lead to the formation well understood, though several mechanisms have been pro- of chromosomes with a lower mutational load compared to posed that may explain how it evolves. First, recombination the ancestral chromosomes. Without recombination, each rates often differ between sexes (Burt et al., 1991), which may chromosome will accumulate mutations over time, mutation- suggest the presence of recombination-suppressor genes as free chromosomes will become increasingly rare, and may postulated by Nei (1969). Such a (local) suppressor gene may eventually be lost due to genetic drift. When such mutation- spread provided that it is linked to a beneficial combination of free chromosomes have been lost, the ratchet has turned a genes (e.g., SD and SA genes). A sex-linked global recombin- single click; compared to the ancestral chromosome, the ation suppressor would explain the marked differences in re- least-loaded chromosome now carries at least one mutation. combination rates between sexes, as this would lead to Subsequent clicks of the ratchet then lead to loss of all reduced recombination in one sex. chromosomes carrying one mutation, etc. Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth 75

Without recombination

With recombination

(a)

Without recombination

With recombination

(b)

Without recombination

With recombination

(c)

Without recombination

With recombination

(d) Legend Chromosome Weakly beneficial mutation Deleterious mutation Strongly beneficial mutation Figure 1 Recombination and chromosomal degeneration. Different models may contribute to degeneration of non-recombining chromosomes. (a) Muller’s ratchet. Mutation-free chromosomes cannot be restored when lost stochastically. (b) Hill–Robertson interference. Beneficial mutations cannot be combined if they arose on different chromosomes. (c) Background selection. Beneficial mutations may not spread if they are linked to deleterious mutations. (d) Genetic hitchhiking. Deleterious mutations may spread when linked to beneficial mutations. See text for further details. Adapted from Bachtrog, D., 2013. Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nature Reviews Genetics 14, 113–124, with permission from Macmillan Publishers Ltd, r 2013.

Hill–Robertson interference refers to the inability to com- genetic background it arose in. Consequently, selection can bine beneficial mutations in the absence of recombination only act on the combined effects of mutations and their re- (Hill and Robertson, 1966). In natural populations, beneficial spective backgrounds (Rice and Chippindale, 2001); beneficial mutations spread as a result of selection. In case such mu- mutations may be lost due to linkage to deleterious mutations tations have not yet become fixed, a novel beneficial mutation (background selection, Charlesworth et al., 1993), whereas may occur on a chromosome which does not yet carry a deleterious mutations may spread when linked to strongly beneficial mutation. Recombination in double heterozygotes beneficial mutations (genetic hitchhiking, Rice, 1987b). may then create a chromosome harboring both beneficial Background selection occurs when a weakly beneficial mutations, whereas without recombination, these mutations mutation is lost because it is unable to overcome the negative will compete with one another (Hill and Robertson, 1966; selection it faces from linked deleterious mutations (Charles- Charlesworth and Charlesworth, 2000). Natural selection will worth et al., 1993; Rice, 1996). An example would be when a then lead to fixation of the more beneficial mutation, effect- weakly beneficial mutation arises on a chromosome already ively purging the other mutation. experiencing a relatively high mutational load due to Muller’s The second effect of recombination, the ability to select on ratchet. Initially, this may spread, but as time progresses, each loci separately, is akin to Hill–Robertson interference. Without copy will only become associated with higher mutational recombination, ancestral combinations cannot give rise to loads as Muller’s ratchet turns. As a result, it will eventually novel combinations and thus each mutation is restricted to the transgress the selection threshold and thus, the beneficial 76 Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth mutation will be lost. With recombination, such a weakly Gene Content of Late-Stage Sex Chromosomes beneficial mutation may end up on a chromosome with a Sex chromosome maturation is associated with major changes smaller load, where it is able to spread due to natural selection. in their gene content. Depending on the genetic mechanism of Inversely, genetic hitchhiking describes how strongly bene- sex determination, variable numbers of sex determination ficial mutations may spread and drag along deleterious mu- genes may be present on the sex chromosomes. Sex de- tations (Rice, 1987b). Similar to the scenario for background termination genes may be single dominant loci such as SRY in selection, it assumes that several weakly deleterious mutations mammals (Berta et al., 1990), or they may represent quanti- may already be present on a chromosome due to Muller’s tative loci that direct sex determination depending on their ratchet. A strongly beneficial mutation on this chromosome dose (e.g., X-linked signal elements as found in Drosophila may still become fixed, provided that its net fitness transcends melanogaster, Cline, 1993). the fitness of chromosomes lacking this mutation, even when Though predicted to play a major role in sex chromosome having a lower deleterious mutation load. This in turn may help evolution, SA genes have proven difficult to be identified. An to accelerate Muller’s ratchet (Bachtrog, 2008); the mutational excessive number of genes involved in male reproductive load of a chromosome may increase, but a strongly beneficial functioning are sexually antagonistic in D. melanogaster mutation reduces the selection pressure on this chromosome. As (Innocenti and Morrow, 2010) and Drosophila miranda (Zhou a result, it spreads through the population, eventually out- and Bachtrog, 2012a). Late-stage sex chromosomes are often competing the ancestral mutation-free chromosome. enriched for genes involved in reproductive processes, such as The effects of these population genetic processes are amp- fertility genes or genes expressed specifically in the gonads lified by the reduced effective population size of the sex (e.g., Skaletsky et al., 2003; Bellott et al., 2010). However, chromosomes (Table 1). The ratio between autosomes and X whether such genes are commonly under sexually antagonistic chromosomes is 4 to 3 per mating pair, whereas this is only 4 selection is unknown and requires further investigation in to 1 for Y chromosomes (and 2 to 1 for both U and V other species. In addition, some sex chromosomes show en- chromosomes; Rice, 1988). This strongly increases the effect of richment for genes that are under sexual selection, such as genetic drift and may further accelerate Muller’s ratchet. color genes in poeciliids (Kallman, 1970), cichlids (Streelman Males typically experience stronger sexual selection than fe- et al., 2003), and medaka fish (Wada et al., 1998). Possibly, males. These effects may be further intensified for the male- such genes represent additional types of SA genes, as they may limited Y and V chromosomes (reviewed in Bachtrog et al., be harmful in females for their increasing conspicuousness. 2011), whereas they may be relatively relaxed on female-limited SD genes or genes that confer large fitness benefits are less U and W chromosomes. However, in UV systems and plants, prone to degeneration. Due to strong selection on these the degeneration of sex chromosomes is often slower compared genes, mutations are more likely to have large deleterious ef- to diploid animals. This is likely due to purifying selection in fects and thus Muller’s ratchet may not operate efficiently, as the haploid phase (Bergero and Charlesworth, 2011; Chibalina natural selection will purge such mutations quickly. However, and Filatov, 2011). In plants, gene expression during meiosis of other genes may degenerate, leading to increased sex-specific sex-linked genes is much higher than in animals, whereas spe- bias in the remaining gene content on the minor sex cies with UV systems are haploid during most of their life cycle chromosome that is typical of late-stage minor sex chromo- (e.g., Ahmed et al.,2014). This would prevent sheltering of somes (Y chromosome masculinization or W chromosome deleterious mutations as seen in diploids, resulting in higher feminization). selection pressure against deleterious mutations, thereby slow- Though sex chromosomes may acquire genes through ing down degeneration (Bergero and Charlesworth, 2011; translocation, they may also lose genes. Typically, this con- Chibalina and Filatov, 2011; Charlesworth, 2013). cerns genes that are located on the major sex chromosome, but are beneficial to or only functional in the heterogametic sex (Wu and Xu, 2003). Genes expressed specifically in the gonads Intralocus Competition and Selective Gene Silencing of the heterogametic sex or genes involved in their gamete production were shown to move away from the major sex The overall genetic inertness of the Y chromosome (and chromosome in several species (e.g., Emerson et al., 2004; likely also the W chromosome, though much less data are Vibranovski et al., 2009). Coupled with the accumulation of available) suggests that its degeneration is associated with SA genes that confer fitness benefits to the homogametic sex, gene inactivation. Gene silencing may readily occur through this leads to feminization, respectively masculinization, of the transpositional inactivation (Steinemann and Steinemann, X and Z chromosomes. 1992, 1998). Though typically deleterious, high mutation rates induced by transposons may allow for rapid inactivation of genes involved in intralocus competition (Rice, 1987b). However, silencing of Y-linked alleles may only be favored if Degeneration-Driven Loss and Turnover of Sex there are no negative dosage effects, or if dosage compensation Chromosomes has readily evolved (Kaiser et al.,2011;seealsoMank, 2013). Some genes may be dosage-sensitive and silencing Y-linked al- Does Degeneration Lead to Loss of the Minor Sex leles without upregulation of X-linked alleles may cause dele- Chromosome? terious effects, preventing gene silencing. The link between the evolution of dosage compensation and mutational silencing of With the plethora of degenerative forces acting upon the Y-linked genes requires further theoretical and empirical study. minor sex chromosome, it has been predicted that the Y Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth 77 chromosome will fade away and eventually be lost (Graves, Sex Chromosome Turnover and SD System Transitions 2006). As a result, males would be lost from the population As degeneration continues, the mutational load of the Y and extinction would be imminent. These predictions are chromosome increases. At some point, sex chromosome however based on several incorrect assumptions. turnover may become selectively favorable compared to re- First, degeneration is not constant. It may be rapid on tention of ancestral sex chromosomes. Such turnovers can young proto-sex chromosomes, but slows down over come about in a variety of ways, such as translocation of the time as gene numbers dwindle (Rice, 1988; Bachtrog, 2008; SD gene to an autosome resulting in a novel proto-sex Hughes et al., 2012). Consequently, the probability that chromosome or fusion of a sex chromosome with an auto- a deleterious mutation occurs becomes increasingly small, some resulting in neo-sex chromosomes. High rates of sex asymptotically approaching zero. Though degeneration may chromosome turnover have been described in fish, reptiles, lead to a highly reduced gene content on the Y chromosome, and amphibians (reviewed in Kikuchi and Hamaguchi, 2013) those genes that remain are usually crucial for male repro- and translocation of the SD gene occurs spontaneously in duction (e.g., Lahn and Page, 1997). These genes are under some species (e.g., Traut, 2010). strong purifying selection and thus, mutations in such genes Turnovers in sex chromosomes are hindered by the fact that may be purged very rapidly, preventing the loss of such genes. the ancestral Y chromosome often contains many male-es- Second, gene content of the Y chromosome need not only sential genes (see also above). Turnover may therefore only decrease (see also Graves, 2006); translocation of genes may occur if the novel Y chromosome confers an especially large increase gene content, though the effect on halting degener- fitness benefit, for example when the SD gene maintains an ation may be limited. The degeneration cycle may be reset association with one or more SA genes (van Doorn and by formation of neo-sex chromosomes by fusion between a Kirkpatrick, 2007). As such, it is still unknown whether the sex chromosome and an autosome. This increases gene spread of novel proto-sex chromosomes occurs when a sex content and allows for partial rejuvenation of the minor determination gene lands next to an SA gene or whether SA sex chromosome (Kitano and Peichel, 2012). Alternatively, genes land next to SD genes. sex chromosome turnover leads to creation of novel sex Additionally, sex chromosome turnover may be caused by chromosomes, effectively resetting the cycle (see also below). changes in sex determination mechanisms induced by meiotic Finally, degeneration may not be as inevitable or irreversible drive (Kozielska et al.,2010). If sex chromosomes exhibit as implied. Novel insights reveal that in many species, sex meiotic drive, sex ratios will become distorted. Balancing sex chromosomes remain homomorphic for extended periods of ratio selection will then favor drive-suppressing mutations or time, suggesting the existence of mechanisms which counteract mutations which cause individuals to develop into the rarer sex. degeneration. In the latter case, this may lead to transitions in sex determin- Barring all else, loss of the Y chromosome need not initiate ation systems and sex chromosome turnover if a different population extinction. The widespread occurrence of X0 sys- chromosome acquires the master sex-determining gene. tems in nature suggests that not all Y chromosomes are es- sential for male development. Such Y chromosomes may be readily lost, provided that any essential genes originally con- tained on the Y chromosome have translocated. Conclusions and Open Questions

Sex chromosomes have their own genomic niche and evolve in Escape from Degeneration and Neo-Sex Chromosomes peculiar ways (Figure 2). Starting as autosomes, they become proto-sex chromosomes when they acquire a sex-determining Several mechanism may allow for sex chromosomes to escape function. They mature as sex chromosomes through a complex the degenerative forces acting upon them. Recombination interplay between SD and SA genes and recombination sup- rates often depend on phenotypic rather than genotypic sex, pression, ultimately resulting in their degeneration. Much of and in some organismal groups, such as amphibians and fish, what we know about sex chromosome evolution is inferred sex reversal may occur occasionally (reviewed in Mank, 2012). from theory. Experimental investigation of sex chromosome In sex-reversed individuals, recombination may occur between evolution has been hampered by lack of tractable systems and the sex chromosomes provided that divergence between the variation within or between closely related species. However, sex chromosomes is still relatively minor. Occasional rounds some promising systems that have recently yielded important of recombination may effectively reverse Muller’s ratchet and new insights are several fish species, such as medaka stop other degenerative processes. Sex reversal may thus (Wada et al., 1998) and sticklebacks (Natri et al., 2013)as function as ‘foundation of youth’ (Perrin, 2009), effectively well as insect species such as houseflies (Hamm et al., 2009; allowing the sex chromosomes to circumvent degeneration Feldmeyer et al., 2008) and Drosophila species (Zhou and and decrease their mutational load. Bachtrog, 2012a, 2012b). Intra-chromosomal recombination is another mechanism The role of SA genes in sex chromosome evolution has that could prevent degeneration of vital genes. The human Y been firmly established by theoretical models, but the empir- chromosome contains eight palindromic regions with dupli- ical evidence is still meager. It is still disputable how wide- cated genes (Skaletsky et al., 2003). Gene conversion by non- spread SA genes are, as they have to date been identified in homologous crossover between these duplicated copies allows only a limited number of species, despite the fact that many for removal of mutations (Rozen et al., 2003), conserving genes are under different selection pressures between the sexes duplicated Y-linked genes and reducing degeneration. (reviewed in Cox and Calsbeek, 2009). 78 Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth

12 11 2

10 3

1

9 4

8 5 7 6

Zone with recombination Female-selected allele Zone with suppressed recombination Male-selected allele Ancestral autosomal gene Decayed ancestral gene Male-determining locus (dominant) Inactivated gene Figure 2 Steps in sex chromosome evolution. Sex chromosomes are derived from autosomes (1), and become proto-sex chromosomes when they acquire a sex-determining function (2). They mature as sex chromosomes as SA genes accumulate and recombination becomes suppressed (3–6). Non-essential genes may decay as they accumulate mutations, leading to reduced functionality (7–8). Decayed genes will be selectively silenced (9–10) and large deletions may lead to chromosome shrinkage (11–12). A novel sex chromosome may be formed when another autosome becomes a proto-sex chromosome, thereby resetting the cycle. Adapted from Bachtrog, D., 2013. Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nature Reviews Genetics 14, 113–124, with permission from Macmillan Publishers Ltd, r 2013.

Comparative genomics may help to discover SA genes and to neo-sex chromosomes of various ages will reveal the extent to determine whether they have been preferentially translocated to which the various processes outlined above contribute to the the sex chromosomes. Alternatively, they may act as landing degeneration of sex chromosomes and may elucidate the sites for new SD genes in the origin of proto-sex chromosomes. interplay between degeneration and dosage compensation Additionally, transcriptomic analyses may reveal differences in (Zhou and Bachtrog, 2012a). gene expression between the sexes, thereby increasing the power The mechanisms of progressive suppression of recombin- to identify SA genes. More empirical testing of SA effects, for ation are not yet well understood. The discovery of novel example by manipulating inheritance of sex chromosomes proto-sex chromosomes and neo-sex chromosomes that still through one sex, will be required to validate the role of SA in sex display recombination may allow for more in-depth analysis chromosome evolution. of how recombination becomes suppressed. Multi-factorial The advent of the omics era has led to the development of a systems such as that of the housefly may be very promising in wide array of tools that may help to further disentangle evo- this respect (Feldmeyer et al., 2008; Scott et al., 2014). lutionary processes of sex chromosomes. Neo-sex chromo- In conclusion, insights in sex chromosome evolution have somes have proven useful in discerning which processes been much progressed over recent years. However, there still is contribute to sex chromosome degeneration (e.g., Zhou and an emphasis on theoretical approaches, while testing these Bachtrog, 2012b; Zhou et al., 2012). Comparisons between theories has proven difficult. With the omics era in full bloom, Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth 79 the field of sex chromosome evolution promises to be an ex- Ellegren, H., Parsch, J., 2007. The evolution of sex-biased genes and the sex-biased citing field of research in which novel insights can readily be gene expression. Nature Reviews Genetics 8, 689–698. fi gained. Emerson, J.J., Kaessman, H., Betran, E., Long, M., 2004. Extensive gene traf con the mammalian X chromosome. Science 303, 537–540. Ericksson, J.W., Quintero, J.J., 2007. Indirect effects of ploidy suggest X See also: Gene Origin, Sex Chromosomes and. Recombination and chromosome dose, not X:A ratio, signals sex in Drosophila. PLoS Biology 5, 2821–2830. Selection. Sex Determination. Sex, Evolution and Maintenance of. Feldmeyer, B., Kozielska, M., Kuijper, B., et al., 2008. Climatic variation and the Sexual Conflict geographical distribution of sex-determining mechanisms in the housefly. Evolutionary Ecology Research 10, 797–809. Gorelick, R., 2003. Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet. Biological Journal of the Linnean Society 80, 353–368. Graves, J., 2006. Sex chromosome specialization and degeneration in mammals. Cell 124, 901–914. References Hamm, R.L., Gao, J.R., Lin, G.G., Scott, J.G., 2009. Selective advantage of IIIM males over YM males in cage competition, mating competition, and pupal Ahmed, S., Cock, J.M., Pessia, E., et al., 2014. A haploid system of emergence in Musca domestica L. (Diptera: Muscidae). Environmental sex determination in the brown alga Ectocarpus sp. Current Biology 24, Entomology 38, 499–504. 1945–1957. Hill, W., Robertson, A., 1966. Effect of linkage on limits to artificial selection. Andolfatto, P., Depaulis, F., Navarro, A., 2001. Inversion polymorphisms and Genetics Research (Cambridge) 8, 269–294. nucleotide variability in Drosophila. Genetics Research (Cambridge) 77, 1–8. Hughes, J.F., Skaletsky, H., Brown, L.G., et al., 2012. Strict evolutionary Bachtrog, D., 2008. The temporal dynamics of processes underlying Y chromosome conservation followed rapid gene loss on human and rhesus Y chromosomes. degeneration. Genetics 179, 1513–1525. Nature 483, 82–U124. Bachtrog, D., 2013. Y-chromosome evolution: Emerging insights into processes of Innocenti, P., Morrow, E.H., 2010. The sexually antagonistic genes of Drosophila Y-chromosome degeneration. Nature Reviews Genetics 14, 113–124. melanogaster. PLoS Biology 8, e1000335. Bachtrog, D., Kirkpatrick, M., Mank, J.E., et al., 2011. Are all sex chromosomes Kaiser, V.B., Zhou, Q., Bachtrog, D., 2011. Nonrandom gene loss from the created equal? Trends in Genetics 27, 350–357. Drosophila miranda neo-Y chromosome. Genome Biology and Evolution 3, Bachtrog, D., Mank, J.E., Peichel, C.L., et al., 2014. Sex determination: Why so 1329–1337. many ways of doing it? PLoS Biology 12, e1001899. Kallman, K., 1970. Sex determination and the restriction of sex-linked pigment Bellott, D.W., Skaletsky, H., Pyntikova, T., et al., 2010. Convergent evolution of patterns to the X and Y chromosome in populations of a poeciliid fish, chicken Z and human X chromosomes by expansion and gene acquisition. Xiphophorus maculatus, from the Belize and Sibun rivers of British Honduras. Nature 466, 612–616. Zoologica 55, 1–16. Bergero, R., Charlesworth, D., 2011. Preservation of the Y transcriptome in a 10- Kikuchi, K., Hamaguchi, S., 2013. Novel sex-determining genes in fish and sex million-year-old plant sex chromosome system. Current Biology 21, chromosome evolution. Developmental Dynamics 242, 339–353. 1470–1474. Kirkpatrick, M., 2010. How and why chromosome inversions evolve. PLoS Berta, P., Hawkins, J.R., Sinclair, A.H., et al., 1990. Genetic evidence equating SRY Biology 8, e1000501. and the testis-determining factor. Nature 348, 448–450. Kirkpatrick, M., Hall, D.W., 2004. Sexual selection and sex linkage. Evolution 58, Beukeboom, L.W., Perrin, N., 2014. The Evolution of Sex Determination. Oxford: 683–691. Oxford University Press. Kitano, J., Peichel, C.L., 2012. Turnover of sex chromosomes and speciation in Burt, A., Bell, G., Harvey, P., 1991. Sex-differences in recombination. Journal of fishes. Environmental Biology of Fishes 94, 549–558. Evolutionary Biology 4, 259–277. Kozielska, M., Weissing, F.J., Beukeboom, L.W., Pen, I., 2010. Segregation Carvalho, A.B., Koerich, L.B., Clark, A.G., 2009. Origin and evolution of Y distortion and the evolution of sex-determining mechanisms. Heredity 104, chromosomes: Drosophila tales. Trends in Genetics 25, 270–277. 100–112. Charlesworth, B., 1978. Model for evolution of Y-chromosomes and dosage Lahn, B., Page, D., 1997. Functional coherence of the human Y chromosome. compensation. Proceedings of the National Academy of Sciences of the United Science 278, 675–680. States of America 75, 5618–5622. Lahn, B., Page, D., 1999. Four evolutionary strata on the human X chromosome. Charlesworth, B., Charlesworth, D., 1978. Model for evolution of dioecy and Science 286, 964–967. gynodioecy. American Naturalist 112, 975–997. Maloisel, L., Rossignol, J., 1998. Suppression of crossing-over by DNA methylation Charlesworth, B., Charlesworth, D., 2000. The degeneration of Y chromosomes. in Ascobolus. Genes & Development. 12, 1381–1389. Philosophical Transactions of the Royal Society of London Series B-Biological Mank, J.E., 2012. Small but mighty: The evolutionary dynamics of W and Y sex Sciences 355, 1563–1572. chromosomes. Chromosome Research 20, 21–33. Charlesworth, B., Morgan, M.T., Charlesworth, D., 1993. The effect of deleterious Mank, J.E., 2013. Sex chromosome dosage compensation: Definitely not for mutations on neutral molecular variation. Genetics 134, 1289–1303. everyone. Trends in Genetics 29, 677–683. Charlesworth, D., 2013. Plant sex chromosome evolution. Journal of Experimental Matsuda, M., Nagahama, Y., Shinomiya, A., et al., 2002. DMY is a Y-specific DM- Botany 64, 405–420. domain gene required for male development in the medaka fish. Nature 417, Charlesworth, D., Charlesworth, B., Marais, G., 2005. Steps in the evolution of 559–563. heteromorphic sex chromosomes. Heredity 95, 118–128. Melamed-Bessudo, C., Levy, A.A., 2012. Deficiency in DNA methylation increases Chibalina, M.V., Filatov, D.A., 2011. Plant Y chromosome degeneration is retarded meiotic crossover rates in euchromatic but not in heterochromatic regions in by haploid purifying selection. Current Biology 21, 1475–1479. Arabidopsis. Proceedings of the National Academy of Sciences of the United Cline, T.W., 1993. The Drosophila sex determination pathway: How do flies count to States of America 109, E981–E988. two? Trends in Genetics 9, 385–390. Muller, H.J., 1918. Genetic variability, twin hybrids and constant hybrids, in a case Cox, R.M., Calsbeek, R., 2009. Sexually antagonistic selection, sexual dimorphism, of balanced lethal factors. Genetics 66, 118–138. and the resolution of intralocus sexual conflict. American Naturalist 173, Muller, H.J., 1964. The relation of recombination to mutational advance. Mutation 176–187. Research 1, 2–9. Demuth, J.P., Flanagan, R.J., Delph, L.F., 2014. Genetic architecture of isolation Natri, H.M., Shikano, T., Merila, J., 2013. Progressive recombination suppression between two species of Silene with sex chromosomes and Haldane’s rule. and differentiation in recently evolved neo-sex chromosomes. Molecular Biology Evolution 68, 332–342. and Evolution 30, 1131–1144. van Doorn, G.S., Kirkpatrick, M., 2007. Turnover of sex chromosomes induced Nei, M., 1969. Linkage modification and sex difference in recombination. Genetics by sexual conflict. Nature 449, 909–912. 63, 681–699. Dübendorfer, A., Hediger, M., Burghardt, G., Bopp, D., 2002. Musca domestica,a Nicolas, M., Marais, G., Hykelova, V., et al., 2005. A gradual process of window on the evolution of sex-determining mechanisms in insects. International recombination restriction in the evolutionary history of the sex chromosomes in Journal of Developmental Biology 46, 75–79. dioecious plants. PLoS Biology 3, 47–56. 80 Sex Chromosome Evolution: Birth, Maturation, Decay, and Rebirth

Otto, S.P., Pannell, J.R., Peichel, C.L., et al., 2011. About PAR: The distinct Streelman, J.T., Albertson, R.C., Kocher, T.D., 2003. Genome mapping of the orange evolutionary dynamics of the pseudoautosomal region. Trends in Genetics 27, blotch colour in cichlid fishes. Molecular Ecology 12, 2465–2471. 358–367. Traut, W., 2010. New Y chromosomes and early stages of sex chromosome Pease, J.B., Hahn, M.W., 2012. Sex chromosomes evolved from independent differentiation: Sex determination in Megaselia. Journal of Genetics 89, ancestral linkage groups in winged insects. Molecular Biology and Evolution 29, 307–313. 1645–1653. Vibranovski, M.D., Lopes, H.F., Karr, T.L., Long, M., 2009. Stage-specific expression Perrin, N., 2009. Sex reversal: A fountain of youth for sex chromosomes? Evolution of Drosophila spermatogenesis suggests that meiotic sex chromosome 63, 3043–3049. inactivation drives genomic relocation of testis-expressed genes. PLoS Genetics Presgraves, D.C., 2008. Sex chromosomes and speciation in Drosophila. Trends in 5, e1000731. Genetics 24, 336–343. Van Doorn, G.S., Kirkpatrick, M., 2010. Transitions between male and female Rice, W., 1984. Sex-chromosomes and the evolution of sexual dimorphism. heterogamety caused by sex-antagonistic selection. Nature 186 (2), 629–645. Evolution 38, 735–742. Wada, H., Shimada, A., Fukamachi, S., et al., 1998. Sex-linked inheritance of the Rice, W., 1987a. The accumulation of sexually antagonistic genes as a selective lf locus in the medaka fish (Oryzias latipes). Zoological Science 15, 123–126. agent promoting the evolution of reduced recombination between primitive Werren, J., Beukeboom, L.W., 1998. Sex determination, sex ratios, and genetic sex-chromosomes. Evolution 41, 911–914. conflict. Annual Reviews of Ecology, Evolution and Systematics 29, 233–261. Rice, W., 1987b. Genetic hitchhiking and the evolution of reduced genetic-activity of Wright, A.E., Harrison, P.W., Montgomery, S.H., et al., 2014. Independent stratum the Y-sex chromosome. Genetics 116, 161–167. formation on the avian sex chromosomes reveals interchromosomal gene Rice, W., 1988. The effect of sex-chromosomes on the rate of evolution. Trends in conversion and predominance of purifying selection on the W chromosome. Ecology & Evolution 3, 2–3. Evolution 68, 3281–3295. Rice, W., 1994. Degeneration of a nonrecombining chromosome. Science 263, Wu, C.I., Xu, E.Y., 2003. Sexual antagonism and X inactivation − The SAXI 230–232. hypothesis. Trends in Genetics 19, 243–247. Rice, W., 1996. Evolution of the Y sex chromosome in animals. Bioscience 46, Zhou, Q., Bachtrog, D., 2012a. Sex-specific adaptation drives early sex chromosome 331–343. evolution in Drosophila. Science 337, 341–345. Rice, W., 1998. Male fitness increases when females are eliminated from gene pool: Zhou, Q., Bachtrog, D., 2012b. Chromosome-wide gene silencing initiates Y Implications for the Y chromosome. Proceedings of the National Academy of degeneration in Drosophila. Current Biology 22, 522–525. Sciences of the United States of America 95, 6217–6221. Zhou, Q., Zhu, H., Huang, Q., et al., 2012. Deciphering neo-sex and B chromosome Rice, W., Chippindale, A., 2001. Sexual recombination and the power of natural evolution by the draft genome of Drosophila albomicans. BMC Genomics 13, selection. Science 294, 555–559. 109. Rice, W., Holland, B., 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behavioral Ecology and Sociobiology 41, 1–10. Roesti, M., Moser, D., Berner, D., 2013. Recombination in the threespine stickleback Further Reading genome − patterns and consequences. Molecular Ecology 22, 3014–3027. Bachtrog, D., Mank, J.E., Peichel, C.L., et al., 2014. Sex determination: Why so Rozen, S., Skaletsky, H., Marszalek, J., et al., 2003. Abundant gene conversion many ways of doing it? PLoS Biology 12, e1001899. between arms of palindromes in human and ape Y chromosomes. Nature 423, Charlesworth, B., Charlesworth, D., 1978. Model for evolution of dioecy and 873–876. gynodioecy. American Naturalist 112, 975–997. Scott, J.G., Warren, W.C., Beukeboom, L.W., et al., 2014. Genome of the housefly, Cox, R.M., Calsbeek, R., 2009. Sexually antagonistic selection, sexual dimorphism, Musca domestica L., a global vector of diseases with adaptations to a septic and the resolution of intralocus sexual conflict. American Naturalist 173, environment. Genome Biology 15, 466. 176–187. Skaletsky, H., Kuroda-Kawaguchi, T., Minx, P., et al., 2003. The male-specific region Kitano, J., Peichel, C.L., 2012. Turnover of sex chromosomes and speciation in of the human Y chromosome is a mosaic of discrete sequence classes. Nature fishes. Environmental Biology of Fishes 94, 549–558. 423, 825−U2. Mank, J.E., 2013. Sex chromosome dosage compensation: Definitely not for Steinemann, M., Steinemann, S., 1992. Degenerating Y-chromosome of Drosophila everyone. Trends in Genetics 29, 677–683. miranda − A trap for retrotransposons. Proceedings of the National Academy of Rice, W., 1987a. The accumulation of sexually antagonistic genes as a selective Sciences of the United States of America 89, 7591–7595. agent promoting the evolution of reduced recombination between primitive sex- Steinemann, M., Steinemann, S., 1998. Enigma of Y chromosome degeneration: chromosomes. Evolution 41, 911–914. Neo-Y and neo-X chromosomes of Drosophila miranda a model for sex Wright, A.E., Harrison, P.W., Montgomery, S.H., et al., 2014. Independent stratum chromosome evolution. Genetica 102 (3), 409–420. formation on the avian sex chromosomes reveals interchromosomal gene Stewart, A.D., Pischedda, A., Rice, W., 2010. Resolving intralocus sexual conflict: conversion and predominance of purifying selection on the W chromosome. Genetic mechanisms and time frame. Journal of Heredity 101, S94–S99. Evolution 68, 3281–3295.