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GENETIC ARCHITECTURE of CONSPECIFIC SPERM PRECEDENCE in ALLONEMOBIUS FASCIATUS and ALLONEMOBIUS SOCIUS AUTHORS: Seth C. B

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GENETIC ARCHITECTURE of CONSPECIFIC SPERM PRECEDENCE in ALLONEMOBIUS FASCIATUS and ALLONEMOBIUS SOCIUS AUTHORS: Seth C. B Genetics: Published Articles Ahead of Print, published on April 15, 2007 as 10.1534/genetics.106.064949 TITLE: GENETIC ARCHITECTURE OF CONSPECIFIC SPERM PRECEDENCE IN ALLONEMOBIUS FASCIATUS AND ALLONEMOBIUS SOCIUS AUTHORS: Seth C. Britch*1, Emma J. Swartout*, Daniel D. Hampton†, Michael L. Draney‡, Jiming Chu§, Jeremy L. Marshall**, and Daniel J. Howard* * Department of Biology, New Mexico State University, Las Cruces, New Mexico 88003 † Duke University School of Medicine, Durham, NC 27706 ‡ Department of Natural and Applied Sciences, University of Wisconsin-Green Bay, Green Bay, Wisconsin 54311 § Health Occupations Program, Dona Ana Branch Community College, Las Cruces, New Mexico 88003 ** Department of Entomology, Kansas State University, Manhattan, KS 66506 1S. C. Britch (current address) USDA-ARS Center for Medical, Agricultural, & Veterinary Entomology 1600/1700 SW 23rd Dr Gainesville, FL 32608 Phone: (352) 374-5737 Fax: (352) 374-5781 E-mail: [email protected] 1 RUNNING HEAD: CONSPECIFIC SPERM PRECEDENCE KEYWORDS: CONSPECIFIC SPERM PRECEDENCE, QTL, BIMODAL HYBRID ZONE, REPRODUCTIVE ISOLATION, SPECIATION, ALLONEMOBIUS CRICKET, CORRESPONDENCE: 1S. C. Britch (current address) USDA-ARS Center for Medical, Agricultural, & Veterinary Entomology 1600/1700 SW 23rd Dr Gainesville, FL 32608 Phone: (352) 374-5737 Fax: (352) 374-5781 E-mail: [email protected] 2 ABSTRACT The evolution of barriers to gene exchange is centrally important to speciation. We used the crickets Allonemobius fasciatus and A. socius to investigate the genetic architecture of conspecific sperm precedence (CSP), a post-insemination prezygotic reproductive barrier. With AFLP markers and controlled crosses we constructed linkage maps and estimated positions of QTL associated with CSP. The majority of QTLs have low to moderate effects, although a few QTLs exist in A. socius with large effects, and the numbers of QTLs are comparable to numbers of genes accounting for species differences in other studies. The QTLs are spread across many unlinked markers, yet QTLs placed with linked markers are on a small number of linkage groups which could reflect the role of the large Allonemobius sex chromosome in prezygotic isolation. Although many QTL had positive effects on conspecific sperm utilization several QTL also exerted negative effects, which could be explained by intraspecific sexual conflict, sperm competition, or epistasis of introgressed genes on novel backgrounds. One unexpected outcome was that A. socius CSP alleles have a stronger effect than those from A. fasciatus in hybrid females, causing hybrids to behave like A. socius with regard to sperm utilization. Implications of this asymmetry in the Allonemobius hybrid zone are discussed. 3 INTRODUCTION Speciation research is currently one of the most dynamic fields in modern biology. As noted by Coyne and Orr (2004), there has been more activity in this area of scientific endeavor over the course of the past 20 years than in the previous 125 years. One interesting characteristic of this burst of activity is that most current studies of speciation focus on the evolution and genetics of reproductive barriers (Coyne and Orr 2004). This focus on reproductive barriers is easy to understand. The evolution of barriers to gene exchange irrevocably separates two lineages and assures their future independence. Hence, the evolution of these barriers is of central importance in every speciation event among sexually reproducing organisms. Enough work has now been done on reproductive barriers that a number of clear patterns have begun to emerge; one of the clearest is the important role played by conspecific sperm precedence in the reproductive isolation of closely related animal species (Howard 1999; Simmons 2001; Coyne and Orr 2004). Conspecific sperm precedence is defined as “the favored utilization of sperm from conspecific males in fertilization when both conspecific and heterospecific males have inseminated a female” (Howard 1999, pp. 110-111). The precedence may occur because conspecific sperm out-compete fertilization-competent heterospecific sperm or because of post-insemination incompatibilities between heterospecific males and females (i.e., non-competitive gametic isolation). Consequently, there are many mechanisms that can underlie such heterospecific disadvantages. Although barriers to fertilization operating at the level of sperm and egg have long been recognized as important in the reproductive isolation of broadcast spawning marine invertebrates 4 (Loeb 1915; Lillie 1921), the importance of post-insemination barriers to fertilization in terrestrial animals did not become apparent until the 1990s. It was not until this period of time that gamete competition studies were regularly incorporated into investigations of reproductive isolation. As a result of these analyses, we now recognize that conspecific sperm precedence isolates closely related species in groups as divergent as vertebrates and insects (Howard and Gregory 1993; Gregory and Howard 1994; Wade et al. 1994; Price 1997; Howard 1999; Price et al. 1999; Brown and Eady 2001; Simmons 2001; Fricke and Arnqvist 2004). An insect group in which conspecific sperm precedence (CSP) has been particularly well- studied is the ground cricket genus Allonemobius. Detailed studies over the course of many years (Benedix and Howard 1991; Howard and Gregory 1993; Howard et al. 1993; Doherty and Howard 1996; Gregory and Howard 1994; Gregory et al. 1998; Howard et al. 1998a,b; Britch et al. 2001) have demonstrated that the strong, but incomplete reproductive isolation between the closely related species A. fasciatus and A. socius is due to a single type of reproductive barrier— CSP. The simplicity of the system, a single barrier to gene exchange isolating two closely related species, is extremely rare among species pairs that have been thoroughly investigated (Coyne and Orr 2004). In this case, should we achieve an understanding of the genetic control of CSP, we will have achieved an understanding of the genetic changes that have given rise to new species. Here we report in detail the results of QTL studies of CSP in A. fasciatus and A. socius, preliminary results of which were published earlier (Howard et al. 2002). Although several studies have looked at other isolating mechanisms through QTL analysis (Bradshaw et al. 1998; 5 MacDonald and Goldstein 1999; Fishman et al. 2002; Tao et al. 2003; Nurnberger et al. 2003), the present study is among the first to document QTLs for conspecific sperm precedence (see also Civetta et al. 2002). The QTL approach allows us to estimate the number and location of genetic factors responsible for a difference between two species in a trait, as well as the magnitude of the effect of each QTL. MATERIALS AND METHODS Although preliminary QTL analyses and a linkage map for A. fasciatus using AFLPs (amplified fragment-length polymorphisms; Vos et al. 1995) were previously described (Howard et al. 2002), since the publication of those results, the Howard Lab has switched from an ABI 377 to an ABI 3100 automated sequencer. Given the ease and speed of analysis of the ABI 3100 and some discrepancies in fragment sizes, we re-analyzed all individuals in the A. fasciatus mapping population, and we analyzed individuals from an A. socius mapping population. In both cases, we used five primer combinations to create AFLP linkage maps, and performed QTL analyses to document linked or unlinked single markers or groups of markers strongly associated with CSP in F2-backcross females. The QTL experiments for both species were similar in protocol and are described here in brief. Field-caught crickets from three focal populations in the East Coast (EC) transect (Figure 1), EC 49 and EC 60A (A. fasciatus, north of mixed populations), and EC 65 (A. socius, south of mixed populations), were brought to the lab and screened for species identity using allozymes (Howard 1983; Howard 1986; Howard and Furth 1986). Screening was necessary due to the presence in both populations of introgressed individuals and cryptic congeners in low 6 frequencies. Following the breeding design shown in Figure 2 we hybridized field-caught A. fasciatus males and A. socius females, and backcrossed F1 females with males from first generation lab-reared parental lines to produce F2-backcross females. For linkage mapping and QTL identification we developed AFLP markers (see below) unique to each species by tracing AFLP fragments through two generations (F1 and F2-backcross) that were absent in individuals of the species to which the backcrossing was done (Figure 2). The QTL trait of interest, conspecific sperm precedence (CSP), was measured by documenting the frequency with which males of the species of interest (A. fasciatus when the introgressed genes in the F2-backcross female were from A. fasciatus and A. socius when the introgressed genes were from A. socius) produced offspring when an F2-backcross female was mated once each to an A. fasciatus male and to an A. socius male (Figure 3). Prior studies of sperm precedence among parental types demonstrated that order of matings has no significant effect on sperm utilization patterns (Howard and Gregory 1993; Gregory and Howard 1994); thus, for the sake of simplicity F2- backcross females in both experiments were mated first to A. fasciatus males and second to A. socius males. All matings were closely observed to ensure that only a single spermatophore was transferred to the female by each male. A period of 24–48 hours was imposed between first and second matings. Females that successfully mated to both males were placed in individual cages and left to oviposit in both soil and cotton media for two weeks, after which they were frozen at –80ºC. Soil medium is provided specifically for oviposition, but females also oviposit in approximately equal frequency (Britch, unpubl. data) in water-soaked cotton provided for dietary moisture. Oviposition media were gradually cooled and exposed to an artificial overwintering period of 3 7 months in a 4ºC constant-temperature room. After overwintering, oviposition media were gradually warmed to room temperature and nymphs were left to emerge in individual family cages.
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