To what degree is the divergent adaptation responsible for life's phenotypic variety also responsible for generating the millions of species that manifest this variation? Theory predicts that ecological divergence among populations should promote reproductive isolation, and recent empirical studies provide support for this hypothesis in a limited number of specific taxa. However, the essential question of whether ecology plays a truly general role in speciation has yet to be systematically evaluated. Here we address this integral issue using an approach that adds an ecological dimension to comparative studies investigating the relationship between reproductive isolation and divergence time. Specifically, we quantify ecological divergence for >500 species pairs from eight plant, invertebrate, and vertebrate taxa and statistically isolate its association with reproductive isolation. This approach demonstrates a highly consistent and significant positive association between ecological divergence and reproductive isolation across taxa. This relationship was also observed across different aspects of ecological divergence and components of reproductive isolation. These findings are highly consistent with the hypothesis that ecological adaptation plays a fundamental and taxonomically general role in promoting reproductive isolation and speciation.comparative methods ͉ Coyne and Orr ͉ divergent adaptation ͉ ecological speciation ͉ genetic distance T he hypothesis that ecological adaptation promotes biological diversification was an important element of early 20th century evolutionary thought. This notion was inherent in the idea that adaptive radiations resulted from access to new ecological resources (1, 2). Verbal models further explained how the adaptive fixation of alternative alleles in ecologically diverging populations might incidentally cause the reproductive isolation (RI) that promotes speciation (3-5). Because models predict that such ecological divergence (ED) can drive speciation in allopatry (3) as well as in sympatry (6), this hypothesis pertains across geographic scenarios. Nonetheless, it has been primarily over the last 15 years that explicit empirical studies of ecology's role in speciation have been conducted on natural populations, providing new insights into the mechanisms by which ED causes RI (6-16). However, although examples of ecologically driven RI in a few individual taxa have begun to accumulate, it remains unclear whether these cases represent the exception, reflecting the nonrandom selection of study taxa, or the rule. That is, the fundamental question of whether ED represents a taxonomically general contributor to speciation remains untested.Addressing this question requires a comparative approach. One powerful comparative approach for the study of speciation was introduced by Coyne and Orr (17,18), who plotted indices of RI against genetic distance using published data from each of dozens of pairs of Drosophila species. Treating molecular genetic distance (GD) as a surrogate for time, t...
We performed a quantitative trait locus (QTL) analysis of epicuticular hydrocarbon variation in 1650 F 2 males from crosses of Baja California and mainland Mexico populations of Drosophila mojavensis cultured on two major host cacti. Principal component (PC) analysis revealed five PCs that accounted for 82% of the total epicuticular hydrocarbon variation. Courtship trials with mainland females were used to characterize hydrocarbon profiles of mated and unmated F 2 males, and logistic regression analysis showed that cactus substrates, two PCs, and a PC by cactus interaction were associated with mating success. Multiple QTLs were detected for each hydrocarbon PC and seven G × E (cactus) interactions were uncovered for the X, second, and fourth chromosomes. Males from the courtship trials and virgins were used, so "exposure to females" was included as a factor in QTL analyses. "Exposed" males expressed significantly different hydrocarbon profiles than virgins for most QTLs, particularly for the two PCs associated with mating success. Ten QTLs showed G × E (exposure) interactions with most resulting from mainland genotypes expressing altered hydrocarbon amounts when exposed to females compared to Baja genotypes. Many cactus × exposure interaction terms detected across QTL and all PCs confirmed that organ pipe-reared males expressed significantly lower hydrocarbon amounts when exposed to females than when reared on agria cactus. Epicuticular hydrocarbon variation in D. mojavensis is therefore a multigenic trait with some epistasis, multiple QTLs exhibited pleiotropy, correlated groups of hydrocarbons and cactus substrates determined courtship success, and males altered their hydrocarbon profiles in response to females.
Few studies have examined genotype by environment (GxE) effects on premating reproductive isolation and associated behaviors, even though such effects may be common when speciation is driven by adaptation to different environments. In this study, mating success and courtship song differences among diverging populations of Drosophila mojavensis were investigated in a two-environment quantitative trait locus (QTL) analysis. Baja California and mainland Mexico populations of D. mojavensis feed and breed on different host cacti, so these host plants were used to culture F 2 males to examine host-specific QTL effects and GxE interactions influencing mating success and courtship songs. Linear selection gradient analysis showed that mainland females mated with males that produced songs with significantly shorter L(long)-IPIs, burst durations, and interburst intervals. Twenty-one microsatellite loci distributed across all five major chromosomes were used to localize effects of mating success, time to copulation, and courtship song components. Male courtship success was influenced by a single detected QTL, the main effect of cactus, and four GxE interactions, whereas time to copulation was influenced by three different QTLs on the fourth chromosome. Multiplelocus restricted maximum likelihood (REML) analysis of courtship song revealed consistent effects linked with the same fourth chromosome markers that influenced time to copulation, a number of GxE interactions, and few possible cases of epistasis. GxE interactions for mate choice and song can maintain genetic variation in populations, but alter outcomes of sexual selection and isolation, so signal evolution and reproductive isolation may be slowed in diverging populations. Understanding the genetics of incipient speciation in D. mojavensis clearly depends on cactus-specific expression of traits associated with courtship behavior and sexual isolation.
Models of speciation‐with‐gene‐flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here, we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced postdivergence gene flow that ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of species divergence which is compatible with theoretical models that posit a role of inversions in speciation with gene flow.
Low concentrations of dietary triacylglycerols including tristearin, triolein, and tripalmitolein, were assessed to determine their effects during egg to pupal stages on adult epicuticular hydrocarbon (EHC) variation in cactophilic Drosophila mojavensis. Triacylglycerols were added singly and in combination at concentrations of 1%, 3%, and 9% to a lipid-free culture medium. Control diets included Carolina Drosophila and lipid-free media. Egg to adult viability was reduced at triacylglycerol concentrations greater than 1%, except for tristearin. Both triolein and tripalmitolein increased EHC amounts to levels similar to those in combination and control diets. Tristearin caused significantly lower quantities of EHCs in adult flies than triolein or tripalmitolein, consistent with previous studies on reduced tristearin assimilation into adult EHCs. We rejected the hypothesis that unsaturated and saturated triacylglycerols were assimilated into unsaturated and saturated adult EHCs, respectively. Since these triacylglycerols comprise a fraction of known lipids in the columnar cacti used for breeding in nature, and EHCs serve as contact pheromones in D. mojavensis, these and other naturally occurring triacylglycerols may provide a direct causal link between host plant use and patterns of chemically mediated mate choice.
The extent of host‐specific genetic variation for two life‐history traits, egg to adult developmental time and viability, and one morphological trait closely tied to fitness, adult thorax size, was exposed by employing a nested half‐sib/full‐sib breeding design with Baja and mainland populations of Drosophila mojavensis recently extracted from nature. This study was motivated by the presence of substantial variation in life histories among populations of D. mojavensis that use the fermenting tissues of particular species of columnar cacti for feeding and breeding in the Sonoran Desert. Full‐sib progeny from all sire‐dam crosses were split into cultures of agria cactus, Stenocereus gummosus, and organ pipe cactus, S. thurberi, to examine patterns of genotype‐by‐environment interaction for these fitness components. Baja flies expressed shorter egg‐to‐adult developmental times, higher viabilities, and smaller body sizes than mainland flies consistent with previous studies. Significant sire and dam components of variance were exposed for developmental time and thorax size. Genotype‐by‐environment interactions were significant at the level of dams for developmental time and nearly significant for viability (P = 0.09). Narrow‐ and broad‐sense heritabilities were influenced by host cactus, sex, and population. No strong pattern of genetic correlation emerged among fitness components suggesting that host‐range expansion has not been accompanied by formation of coadapted life histories, yet the ability to estimate genetic correlations and their standard errors was compromised by the unbalanced nature of the data set. Genetic correlations in performance across cacti were slightly positive, evidence for ecological generalism among populations explaining the observed pattern of multiple host cactus use within the species range of D. mojavensis.
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