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Strong Natural Selection on Juveniles Maintains a Narrow Adult Hybrid Zone in a Broadcast Spawner

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Strong Natural Selection on Juveniles Maintains a Narrow Adult Hybrid Zone in a Broadcast Spawner vol. 184, no. 6 the american naturalist december 2014 Strong Natural Selection on Juveniles Maintains a Narrow Adult Hybrid Zone in a Broadcast Spawner Carlos Prada* and Michael E. Hellberg Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 Submitted April 28, 2014; Accepted July 8, 2014; Electronically published October 17, 2014 Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.983b0. year, cumulative effects over many years before reproduc- abstract: Natural selection can maintain and help form species tion begins can generate a strong ecological filter against across different habitats, even when dispersal is high. Selection against inferior migrants (immigrant inviability) acts when locally adapted immigrants. Immigrant inviability can act across environ- populations suffer high mortality on dispersal to unsuitable habitats. mental gradients, generating clines or hybrid zones. If re- Habitat-specific populations undergoing divergent selection via im- productive isolation occurs as a by-product of immigrant migrant inviability should thus show (1) a change in the ratio of inviability, new species can arise by natural selection (Dar- adapted to nonadapted individuals among age/size classes and (2) a win 1859; Nosil et al. 2005; Rundle and Nosil 2005; Schlu- cline (defined by the environmental gradient) as selection counter- ter 2009), often occurring across environmental gradients, balances migration. Here we examine the frequencies of two depth- segregated lineages in juveniles and adults of a Caribbean octocoral, where they generate hybrid zones (Endler 1977). Eunicea flexuosa. Distributions of the two lineages in both shallow The segregation of adults of different species into dif- and deep environments were more distinct when inferred from adults ferent habitats is pronounced in many long-lived, sessile than juveniles. Despite broad larval dispersal, we also found an ex- species with large dispersal, such as wind-pollinated trees tremely narrow hybrid zone (!100 m), with coincident clines for (Paine et al. 2009; Baldeck et al. 2013) and reef corals that molecular and morphological characters of the host coral and its disperse via planktonic larvae (Goreau 1959; Kinzie 1973), algal symbiont. Effective dispersal estimates derived from the hybrid zone are remarkably small (!20 m) for a broadcast spawner. The but whether such segregation arises before or after re- large selection coefficient against mismatched genotypes derived from cruitment remains unknown. Reciprocal transplant ex- cohort data is consistent with that from field transplant experiments. periments show that adults suffer higher mortality in their Narrow hybrid zones and limited effective dispersal may be a com- nonnative habitat (Lowry et al. 2008; Marshall et al. 2010; mon outcome of long periods of postsettlement, prereproductive Prada and Hellberg 2013). These studies show that adap- selection across steep ecological gradients. Strong diversifying selec- tive divergence occurs and that selection can be strong, tion provides a mechanism to explain the prevalence of depth-seg- regated sibling species in the sea. but the extent to which they reveal anything about the role of immigrant inviability in speciation depends on Keywords: prereproductive selection, microgeographic adaptation, prerecruitment processes and whether reproductive iso- octocoral, immigrant inviability. lation is complete. Prerecruitment process, such as larval habitat choice Introduction (Connell 1972; Grosberg 1982), may cause a pattern of habitat segregation in adult populations without immi- Natural selection via immigrant inviability occurs when grant inviability. Larval habitat choice is pronounced in the propagules of locally adapted populations suffer high many sessile marine organisms (Carlon 2002; Baird et al. mortality on migrating to unsuitable habitats (Nosil et al. 2003), particularly in intertidal habitats (Grosberg 1982). 2005; Rundle and Nosil 2005). Immigrant inviability can Pre- and postrecruitment processes are not mutually ex- be pronounced in organisms where the interval between clusive, however, and while larvae may prefer a particular recruitment and sexual reproduction is long, as in corals habitat, subsequent immigrant inviability may still operate and trees (Prada and Hellberg 2013; Lindtke et al. 2014). to more completely segregate adults. Indeed, the two pro- While the effects of selection may be small over any given cesses are interrelated, and postrecruitment mortality * Corresponding author; e-mail: [email protected]. should favor habitat choice by larvae over evolutionary time (Grosberg 1981). If larvae choose their habitat and Am. Nat. 2014. Vol. 184, pp. 702–713. ᭧ 2014 by The University of Chicago. 0003-0147/2014/18406-55454$15.00. All rights reserved. subsequent mortality is independent of habitat, then the DOI: 10.1086/678403 distribution of species across habitats will be similar across This content downloaded from 130.39.115.189 on Tue, 2 Dec 2014 12:04:59 PM All use subject to JSTOR Terms and Conditions Selection against Juvenile Migrants 703 age classes. In contrast, immigrant inviability will result Methods in different distributions between age or size classes, as Biology of Eunicea flexuosa selection weeds out maladapted recruits over time. The distribution of different age/size classes across habitats can Eunicea flexuosa is a colonial marine cnidarian that lives thus provide evidence as to whether pre- or postrecruit- in association with algae of the genus Symbiodinium. Bush- ment mortality drives adult habitat segregation and like colonies 1–1.5 m tall form by the asexual budding of whether and to what degree immigrant inviability works. polyps (Bayer 1961). Colonies acquire their algal symbi- Immigrant inviability should also generate narrow hy- onts from the environment at the single-polyp stage shortly after larval metamorphosis (Coffroth et al. 2001). brid zones because selection acts across environmental gra- Eunicea flexuosa comprises two depth-segregated lineages, dients (Endler 1975, 1977; Slatkin 1975). Habitat-mediated each adapted to its own depth as inferred from reciprocal selection may be acute in organisms in which dispersal transplants (Prada et al. 2008; Prada and Hellberg 2013). potential exceeds the scale of environmental change (En- Each lineage maintains its own algal symbiont phylotype, dler 1979), such as wind-pollinated plants and marine even when both lineages meet at intermediate depths broadcasters with pelagic larvae. A long period (tens of (Prada et al. 2014). Colonies of E. flexuosa have separate years) between dispersal and the onset of reproduction sexes, and sexual reproduction occurs through spawning should enhance the opportunity for selection to sort in- of gametes that are fertilized in the water column (Beiring dividuals by habitat before they reproduce (Prada and and Lasker 2000). Sperm and eggs are positively buoyant Hellberg 2013), thereby reducing the formation of hybrids. and, after release, rise to the surface, where fertilization The candelabrum coral Eunicea flexuosa is an especially more readily occurs (C. Prada, personal observation). As suitable species in which to evaluate the role of immigrant in other octocorals, most fertilization takes place within inviability in the segregation of lineages across habitats 30 min of gamete release (Alino and Coll 1989). In the (depths) because (1) different selective regimes associated closely related broadcast spawner Plexaura kuna, most with variation in depth occur at far smaller scales than mating occurs between neighboring colonies, but at least dispersal, which appears to approximate panmixia across 8% of fertilization events involves colonies 120 m apart the Caribbean (Prada and Hellberg 2013); (2) first repro- (Coffroth and Lasker 1998). Gametes remain viable for at least 2 h after release in other free-spawning Caribbean duction does not occur until 130 years of age (Beiring and anthozoans (Lasker et al. 1996; Levitan 2004). In Obicella Lasker 2000); and (3) unlike other reef taxa, fragmentation annularis, which co-occurs with E. flexuosa,eggsmoveon is uncommon, and age can accurately be estimated from average 1500 m, and not less than 100 m, in 100 min size, making comparisons across age classes easier. Pre- (Levitan et al. 2004). Thus, in !2heggscommonlydisperse viously, we suggested that immigrant inviability might op- distances greater than the transition separating shallow and erate on habitat-segregated lineages of E. flexuosa because deep forms (!100 m). reciprocally transplanted adult colonies revealed adaptive Larvae develop planktonically, and larval dispersal ap- differences between genetically differentiated shallow and pears to be high; widely separated (11,000 km) locations deep populations (Prada et al. 2008; Prada and Hellberg form panmictic populations (Prada and Hellberg 2013). 2013). Here we compare the distribution of these lineages Isolation with migration analyses suggest some introgres- in adults and juveniles at the extremes of a depth gradient sion between the shallow and deep lineages (Prada and in Puerto Rico. We find that while the lineages in both Hellberg 2013), but whether migration is ongoing was size classes are sorted by habitat, segregation is more pro- heretofore unknown. nounced in adults. We also found that the two lineages replace each other over a depth and light gradient, pro- Sampling and Sequence Data ducing few hybrids. Clines for three morphological
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