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Genetic Architecture of Conspecific Sperm Precedence In Copyright Ó 2007 by the Genetics Society of America DOI: 10.1534/genetics.106.064949 Genetic Architecture of Conspecific Sperm Precedence in Allonemobius fasciatus and A. socius 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, North Carolina 27706, ‡Department of Natural and Applied Sciences, University of Wisconsin, Green Bay, Wisconsin 54311, §Health Occupations Program, Dona Ana Branch Community College, Las Cruces, New Mexico 88003 and **Department of Entomology, Kansas State University, Manhattan, Kansas 66506 Manuscript received August 17, 2006 Accepted for publication April 1, 2007 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 postinsemination prezygotic reproductive barrier. With amplified fragment-length polymor- phism (AFLP) markers and controlled crosses we constructed linkage maps and estimated positions of QTL associated with CSP. The majority of QTL have low to moderate effects, although a few QTL exist in A. socius with large effects, and the numbers of QTL are comparable to numbers of genes accounting for species differences in other studies. The QTL are spread across many unlinked markers, yet QTL placed with linked markers are on a small number of linkage groups that 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. PECIATION research is currently one of the most lization of sperm from conspecific males in fertilization S dynamic fields in modern biology. As noted by when both conspecific and heterospecific males have Coyne and Orr (2004), there has been more activity in inseminated a female’’ (Howard 1999, pp. 110–111). this area of scientific endeavor over the course of the The precedence may occur because conspecific sperm past 20 years than in the previous 125 years. One in- outcompete fertilization-competent heterospecific sperm teresting characteristic of this burst of activity is that or because of postinsemination incompatibilities be- most current studies of speciation focus on the evo- tween heterospecific males and females (i.e., non- lution and genetics of reproductive barriers (Coyne competitive gametic isolation). Consequently, there are and Orr 2004). This focus on reproductive barriers is many mechanisms that can underlie such heterospe- easy to understand. The evolution of barriers to gene cific disadvantages. exchange irrevocably separates two lineages and assures Although barriers to fertilization operating at the their future independence. Hence, the evolution of level of sperm and egg have long been recognized as these barriers is of central importance in every spe- important in the reproductive isolation of broadcast- ciation event among sexually reproducing organisms. spawning marine invertebrates (Loeb 1915; Lillie Enough work has now been done on reproductive 1921), the importance of postinsemination barriers to barriers that a number of clear patterns have begun to fertilization in terrestrial animals did not become ap- emerge; one of the clearest is the important role played parent until the 1990s. It was not until this period of by conspecific sperm precedence in the reproductive time that gamete competition studies were regularly isolation of closely related animal species (Howard incorporated into investigations of reproductive iso- 1999; Simmons 2001; Coyne and Orr 2004). Conspe- lation. As a result of these analyses, we now recognize cific sperm precedence is defined as ‘‘the favored uti- that conspecific sperm precedence isolates closely re- lated species in groups as divergent as vertebrates and insects (Howard and Gregory 1993; Gregory and Howard 1994; Wade et al. 1994; Price 1997; Howard 1Corresponding author: USDA-ARS, Center for Medical, Agricultural, and rice rown ady immons Veterinary Entomology, 1600/1700 SW 23rd Dr., Gainesville, FL 32608. 1999; P et al. 1999; B and E 2001; S E-mail: [email protected] 2001; Fricke and Arnqvist 2004). Genetics 176: 1209–1222 ( June 2007) 1210 S. C. Britch et al. An insect group in which conspecific sperm pre- tion we developed AFLP markers (see below) unique to each cedence (CSP) has been particularly well studied is the species by tracing AFLP fragments through two generations ground cricket genus Allonemobius. Detailed studies (F1 and F2 backcross) that were absent in individuals of the enedix oward species to which the backcrossing was done (Figure 2). over the course of many years (B and H The QTL trait of interest, CSP, was measured by documenting 1991; Howard and Gregory 1993; Howard et al. 1993; the frequency with which males of the species of interest (A. Gregory and Howard 1994; Doherty and Howard fasciatus when the introgressed genes in the F2-backcross 1996; Gregory et al. 1998; Howard et al. 1998a,b; female were from A. fasciatus and A. socius when the intro- Britch et al. 2001) have demonstrated that the strong, gressed genes were from A. socius) produced offspring when an F2-backcross female was mated once each to an A. fasciatus but incomplete reproductive isolation between the male and to an A. socius male (Figure 3). Prior studies of sperm closely related species Allonemobius fasciatus and A. socius precedence among parental types demonstrated that order of is due to a single type of reproductive barrier—CSP. The matings has no significant effect on sperm utilization patterns simplicity of the system, a single barrier to gene exchange (Howard and Gregory 1993; Gregory and Howard 1994); isolating two closely related species, is extremely rare thus, for the sake of simplicity F2-backcross females in both experiments were mated first to A. fasciatus males and second among species pairs that have been thoroughly investi- to A. socius males. All matings were closely observed to ensure gated (Coyne and Orr 2004). In this case, should we that only a single spermatophore was transferred to the female achieve an understanding of the genetic control of CSP, by each male. A period of 24–48 hr was imposed between first we will have achieved an understanding of the genetic and second matings. changes that have given rise to new species. Females that successfully mated to both males were placed in individual cages and left to oviposit in both soil and cotton Here we report in detail the results of QTL studies of media for 2 weeks, after which they were frozen at À80°. Soil CSP in A. fasciatus and A. socius, preliminary results of medium is provided specifically for oviposition, but females which were published earlier (Howard et al. 2002). Al- also oviposit in approximately equal frequency (S. C. Britch, though several studies have looked at other isolating unpublished data) in water-soaked cotton provided for dietary mechanisms through QTL analysis (Bradshaw et al. moisture. Oviposition media were gradually cooled and ex- posed to an artificial overwintering period of 3 months in a 4° 1998; MacDonald and Goldstein 1999; Fishman et al. ao urnberger constant-temperature room. After overwintering, oviposition 2002; T et al. 2003; N et al. 2003), this study media were gradually warmed to room temperature and is among the first to document QTL for conspecific nymphs were left to emerge in individual family cages. When sperm precedence (see also Civetta et al. 2002). The nymphs reached second or third instar they were frozen en QTL approach allows us to estimate the number and masse at À80° to await paternity analysis, which was accom- plished with allozyme phenotyping. The resulting data were location of genetic factors responsible for a difference used to determine the pattern of sperm utilization by each F2- between two species in a trait, as well as the magnitude of backcross female, in particular the frequency with which each the effect of each QTL. male fathered offspring. AFLP typing of parents, males, F1 females, and F2-backcross females was done post hoc, since many females were expected MATERIALS AND METHODS to either not complete a second mating or not mate at all; similarly, many males will not mate in the laboratory. Following Although preliminary QTL analyses and a linkage map for restriction ligations of cricket genomic DNA, extracted using A. fasciatus using amplified fragment-length polymorphisms QIAGEN (Valencia, CA) DNEasy kits (no. 69504), we used the (AFLPs) (Vos et al. 1995) were previously described (Howard ABI Regular Genome mapping kit (no. 4303050) to do pre- et al. 2002), since the publication of those results, the Howard selective and selective PCR amplification of samples, which Lab has switched from an ABI 377 to an ABI 3100 automated were then run on the ABI 3100 sequencer. A prior survey ( J. L. sequencer. Given the ease and speed of analysis of the ABI Marshall, unpublished data) identified five combinations of 3100 and some discrepancies in fragment sizes, we reanalyzed selective amplification primers that consistently produced all individuals in the A. fasciatus mapping population, and $70 AFLP fragments per individual. We code these combina- we analyzed individuals from an A. socius mapping popula- tions here as B5, B6, G3, G7, and H5, but primer names as well tion. In both cases, we used five primer combinations to create as all molecular protocols are available from the correspond- AFLP linkage maps and performed QTL analyses to document ing author.
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