Article

Adaptive Evolution of Bindin in the Genus Heliocidarus is Correlated with the Shift to Direct Development

Smithsonian Tropical Research Institute, Box 2072, Balboa, Panama.
Evolution (Impact Factor: 4.66). 11/2003; 57(10):2293-302. DOI: 10.1554/02-671
Source: PubMed

ABSTRACT Sea urchins are widely used to study both fertilization and development. In this study we combine the two fields to examine the evolution of reproductive isolation in the genus Heliocidaris. Heliocidaris tuberculata develops indirectly via a feeding larva, whereas the only other species in the genus, H. erythrogramma, has evolved direct development through a nonfeeding larva. We estimated the time of divergence between H. erythrogramma and H. tuberculata from mitochondrial DNA divergence, quantified levels of gametic compatibility between the two species in cross-fertilization assays, and examined the mode of evolution of the sperm protein bindin by sequencing multiple alleles of the two species. Bindin is the major component of the sea urchin sperm acrosomal vesicle, and is involved in sperm-egg attachment and fusion. Based on our analyses, we conclude that: the two species of Heliocidaris diverged less than five million years ago, indicating that direct development can evolve rapidly in sea urchins; since their divergence, the two species have become gametically incompatible; Heliocidaris bindin has evolved under positive selection; and this positive selection is concentrated on the branch leading to H. erythrogramma. Three hypotheses can explain the observed pattern of selection on bindin: (1) it is a correlated response to the evolution of direct development in H. erythrogramma; (2) it is the result of an intraspecific process acting in H. erythrogramma but not in H. tuberculata; or (3) it is the product of reinforcement on the species that invests more energy into each egg to avoid hybridization.

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    • "Patterns of bindin divergence between these subspecies were therefore described qualitatively for each region. We added all Western Australian haplotypes to the Eastern Australian Heliocidaris bindin phylogeny generated by Zigler et al. (2003) to determine where these Western Australian subspecies fit in the Heliocidaris genus, particularly for comparison with our CO1 phylogeny. We used PAUP * version 4.0b10 (Swofford 2003) to regenerate the phylogeny using the substitution model of Tamura and Nei (1993) with gamma correction and 9999 iterations for bootstrap support by neighbor joining methods. "
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    ABSTRACT: The evolution of reproductive barriers is crucial to the process of speciation. In the Echinoidea, studies have focused on divergence in the gamete recognition protein, bindin, as the primary isolating mechanism among species. As such, the capacity of alternate mechanisms to be effective reproductive barriers and the phylogenetic context in which they arise is unclear. Here, we examine the evolutionary histories and factors limiting gene exchange between two subspecies of Heliocidaris erythrogramma that occur sympatrically in Western Australia. We found low, but significant differentiation between the subspecies in two mitochondrial genes. Further, coalescent analyses suggest that they diverged in isolation on the east and west coasts of Australia, with a subsequent range expansion of H. e. erythrogramma into Western Australia. Differentiation in bindin was minimal, indicating gamete incompatibility is an unlikely reproductive barrier. We did, however, detect strong asynchrony in spawning seasons; H. e. erythrogramma spawned over summer whereas H. e. armigera spawned in autumn. Taken together, we provide compelling evidence for a recent divergence of these subspecies and their reproductive isolation without gamete incompatibility. Western Australian H. erythrogramma may therefore present an intriguing case of incipient speciation, which depends on long-term persistence of the factors underlying this spawning asynchrony.
    Evolution 11/2012; 66(11):3545-57. DOI:10.1111/j.1558-5646.2012.01700.x · 4.66 Impact Factor
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    • "Patterns of bindin divergence between these subspecies were therefore described qualitatively for each region. We added all Western Australian haplotypes to the Eastern Australian Heliocidaris bindin phylogeny generated by Zigler et al. (2003) to determine where these Western Australian subspecies fit in the Heliocidaris genus, particularly for comparison with our CO1 phylogeny. We used PAUP * version 4.0b10 (Swofford 2003) to regenerate the phylogeny using the substitution model of Tamura and Nei (1993) with gamma correction and 9999 iterations for bootstrap support by neighbor joining methods. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Data Archived: doi:10.5061/dryad.1b549 The evolution of reproductive barriers is crucial to the process of speciation. In the Echinoidea, studies have focused on divergence in the gamete recognition protein, bindin, as the primary isolating mechanism among species. As such, the capacity of alternate mechanisms to be effective reproductive barriers and the phylogenetic context in which they arise is unclear. Here, we examine the evolutionary histories and factors limiting gene exchange between two subspecies of Heliocidaris erythrogramma that occur sympatrically in Western Australia. We found low, but significant differentiation between the subspecies in two mitochondrial genes. Further, coalescent analyses suggest that they diverged in isolation on the east and west coasts of Australia, with a subsequent range expansion of H. e. erythrogramma into Western Australia. Differentiation in bindin was minimal, indicating gamete incompatibility is an unlikely reproductive barrier. We did, however, detect strong asynchrony in spawning seasons; H. e. erythrogramma spawned over summer whereas H. e. armigera spawned in autumn. Taken together, we provide compelling evidence for a recent divergence of these subspecies and their reproductive isolation without gamete incompatibility. Western Australian H. erythrogramma may therefore present an intriguing case of incipient speciation, which depends on long-term persistence of the factors underlying this spawning asynchrony. K E Y W O R D S : Heliocidaris erythrogramma armigera, reproductive isolation, speciation. The process of speciation is initiated by barriers to gene ex-change, which over time lead to the accumulation of genetic differences and reproductive isolation (Mayr 1942, 1963). Ini-tial barriers to gene flow can arise by geographic displacement (i.e., allopatry), through biological, topographic, or oceano-graphic limitations to dispersal (e.g., Lessios et al. 2001; Johnson and Black 2006; Sherman et al. 2008), or in the same geographic location (i.e., sympatry) through ecological shifts and habitat spe-cialization (e.g., Feder et al. 1988; Barluenga et al. 2006). Fol-lowing extended periods of isolation and subsequent genetic dif-ferentiation, a variety of reproductive barriers can arise, which can be split into two categories: prezygotic barriers, which reduce the opportunity or ability for gametes to successfully fertilize, and postzygotic barriers, which impact the fitness of hybrid off-spring, either through impaired survival or sterility (Mayr 1963; Dobzhansky 1970). Studying these barriers in recently diverg-ing groups can provide considerable insight into the evolutionary processes leading to speciation. Marine species, particularly broadcast spawners, have been especially well studied in the context of understanding the evo-lution of prezygotic reproductive barriers owing to the ease of gamete access and manipulation (Palumbi 1994; Lessios 2007). In such species, reproductive isolation can arise in the form of temporal barriers by asynchronies in the timing of spawning 1 C 2012 The Author(s). Evolution
    Evolution 01/2012; DOI:10.2307/23273891 · 4.66 Impact Factor
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    • "Intraspecific and interspecific variation of the bindin locus has been studied in seven genera of sea urchins: Echinometra (Metz and Palumbi 1996; McCartney and Lessios 2004), Strongylocentrotus (Biermann 1998), Arbacia (Metz et al. 1998a), Tripneustes (Zigler and Lessios 2003b), Heliocidaris (Zigler et al. 2003) Lytechinus (Zigler and Lessios 2004), and Paracentrotus (Calderon et al. 2009, 2010). In the absence of information regarding variation in the bindin receptor EBR1, studies of bindin have used sequences of bindin in females as a proxy, even though bindin is a sex-limited gene. "
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    ABSTRACT: Research on speciation of marine organisms has lagged behind that of terrestrial ones, but the study of the evolution of molecules involved in the adhesion of gametes in free-spawning invertebrates is an exception. Here I review the function, species-specificity, and molecular variation of loci coding for bindin in sea urchins, lysin in abalone and their egg receptors, in an effort to assess the degree to which they contribute to the emergence of reproductive isolation during the speciation process. Bindin is a protein that mediates binding of the sperm to the vitelline envelope (VE) of the egg and the fusion of the gametes' membranes, whereas lysin is a protein involved only in binding to the VE. Both of these molecules are important in species recognition by the gametes, but they rarely constitute absolute blocks to interspecific hybridization. Intraspecific polymorphism is high in bindin, but low in lysin. Polymorphism in bindin is maintained by frequency-dependent selection due to sexual conflict arising from the danger of polyspermy under high densities of sperm. Monomorphism in lysin is the result of purifying selection arising from the need for species recognition. Interspecific divergence in lysin is due to strong positive selection, and the same is true for bindin of four out of seven genera of sea urchins studied to date. The differences between the sea urchin genera in the strength of selection can only partially be explained by the hypothesis of reinforcement. The egg receptor for lysin (VERL) is a glycoprotein with 22 repeats, 20 of which have evolved neutrally and homogenized by concerted evolution, whereas the first two repeats are under positive selection. Selection on lysin has been generated by the need to track changes in VERL, permitted by the redundant structure of this molecule. Both lysin and bindin are important in reproductive isolation, probably had a role in speciation, but it is hard to determine whether they meet the strictest criteria of "speciation loci," defined as genes whose differentiation has caused speciation.
    Integrative and Comparative Biology 06/2011; 51(3):456-65. DOI:10.1093/icb/icr039 · 2.97 Impact Factor
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