The rapid evolution of sexual isolation in sympatry has long been associated with reinforcement (i.e., selection to avoid maladaptive hybridization). However, there are
many species pairs in sympatry that have evolved rapid sexual isolation without known
costs to hybridization. A major unresolved question is what evolutionary processes are
involved in driving rapid speciation in such cases. Here, we focus on one such system;
the Drosophila athabasca species complex, which is composed of three partially sympatric and interfertile semispecies: WN, EA, and EB. To study speciation in this species
complex, we assayed sexual and genomic isolation within and between these semispecies in both sympatric and allopatric populations. First, we found no evidence of reproductive character displacement (RCD) in sympatric zones compared to distant
allopatry. Instead, semispecies were virtually completely sexually isolated from each
other across their entire ranges. Moreover, using spatial approaches and coalescent
demographic simulations, we detected either zero or only weak heterospecific gene
flow in sympatry. In contrast, within each semispecies we found only random mating
and little population genetic structure, except between highly geographically distant
populations. Finally, we determined that speciation in this system is at least an order
of magnitude older than previously assumed, with WN diverging first, around
200K years ago, and EA and EB diverging 100K years ago. In total, these results suggest that these semispecies should be given full species status and we adopt new nomenclature: WN—D. athabasca, EA—D. mahican, and EB—D. lenape. While the lack of
RCD in sympatry and interfertility do not support reinforcement, we discuss what
additional evidence is needed to further decipher the mechanisms that caused rapid
speciation in this species complex.
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An experimental test of the evolutionary consequences of sympatry in Drosophila subquinaria
Prezygotic isolation is often stronger between sympatric as opposed to allopatric taxa, but the underlying cause can be difficult to infer from comparative studies alone. Experimental evolution, where evolutionary responses to treatments manipulating the presence/absence of heterospecific individuals are tracked, can provide a powerful complementary approach. We used experimental evolution to investigate a naturally occurring pattern of reproductive character displacement in the mushroom-feeding fly, Drosophila subquinaria. In nature, female D. subquinaria from populations sympatric with the closely related Drosophila recens discriminate more strongly against heterospecific males than do females from allopatric populations. Starting with 16 replicate allopatric populations of D. subquinaria, we manipulated the presence/absence of D. recens during mating (experimental sympatry vs. control) and, when present, we allowed hybrids to live or kill them each generation. Across 12 generations, heterospecific offspring production from no-choice mating trials between D. subquinaria females and D. recens males declined in both experimental sympatry treatments relative to the control, suggesting increased sexual isolation. Male cuticular hydrocarbon profiles also evolved, but only in the hybrids killed treatment. Our results strongly imply that the existing reproductive character displacement in wild D. subquinaria populations was an evolutionary response to selection arising from secondary contact with D. recens.
more » « less- NSF-PAR ID:
- 10493203
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- Volume:
- 78
- Issue:
- 3
- ISSN:
- 0014-3820
- Format(s):
- Medium: X Size: p. 555-565
- Size(s):
- ["p. 555-565"]
- Sponsoring Org:
- National Science Foundation
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Abstract When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species
Drosophila subquinaria andDrosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine‐scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. WithinD. subquinaria , reinforcement is extremely effective: we find variation in mate discrimination both againstD. recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression fromD. recens . InD. recens , we do not find evidence for increased mate discrimination in sympatry, even whereD. recens is rare, consistent with substantial gene flow throughout the species’ range. Finally, we find that introgression between species is asymmetric, with more fromD. recens intoD. subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement withinD. subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations. -
• Reinforcement is the process through which prezygotic reproductive barriers evolve in sympatry due to selection against hybridization between co-occurring, closely related species. The role of self-fertilization in reinforcement and reproductive isolation is uncertain in part because its efficiency as a barrier against heterospecific mating can depend on the timing of autonomous selfing. • To investigate whether increased autonomous selfing has evolved as a mechanism for reinforcement, we compared Phlox cuspidata populations across their native Texas range using both estimates of genetic diversity and experimental manipulation with morphological measurements. Specifically, we investigated patterns of variation in floral traits and timing of selfing between individuals from allopatric populations of P. cuspidata and from populations sympatric with the closely related species, P. drummondii. • We infer intermediate rates of selfing across field-collected individuals with no significant difference between allopatric and sympatric populations. Among greenhouse grown plants, we find no differences in timing of selfing or other floral traits including anther dehiscence timing, anther-stigma distances, autonomous selfing rate and self-seed count between allopatric and sympatric populations. However, our statistical analyses indicate that P. cuspidata individuals sympatric with P drummondii seem to have generally larger flowers compared to allopatric individuals. • Despite strong evidence of costly hybridization with P. drummondii, we find no evidence of trait divergence due to reinforcement in P. cuspidata. Although we document nearly complete autonomous self-seed set in the greenhouse, estimates of selfing rates from genetic data imply realized selfing is much lower in nature suggesting an opportunity for reinforcing selection to act on this trait.more » « less
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Abstract Premise Many tropical plants are bat‐pollinated, but these mammals often carry copious, multispecific pollen loads making bat‐pollinated plants susceptible to heterospecific pollen deposition and reproductive interference. We investigated pollen transfer between sympatric bat‐pollinated Burmeistera species and their response to heterospecific pollen deposition from each other. Methods We quantified conspecific and heterospecific pollen deposition for two populations of B. ceratocarpa , a recipient species in heterospecific pollen transfer interactions, that co‐occur with different donor relatives ( B. borjensis and B. glabrata ). We then used a cross‐pollination scheme using pollen mixtures to assess the species' responses to heterospecific pollen deposition in terms of fruit abortion and seed production. Results Burmeistera ceratocarpa received significantly more heterospecific pollen from its relatives at both sites than its own pollen was deposited on its relatives. However, heterospecific pollen deposition only affected seed production by B. borjensis and B. glabrata , but not by B. ceratocarpa , suggesting that early acting post‐pollination barriers buffer the latter against reproductive interference. Crosses between sympatric and allopatric populations suggest that the study species are fully isolated in sympatry, while isolation between allopatric populations is strong but incomplete. Conclusions We did not observe evidence of reproductive interference among our study species, because either heterospecific pollen deposition did not affect their seed production ( B. ceratocarpa ) or they receive heterospecific pollen only rarely ( B. borjensis and B. glabrata ). Frequent heterospecific pollen deposition might favor the evolution of barriers against foreign pollen (as in B. ceratocarpa ) that alleviate the competitive costs of sharing low fidelity pollinators with co‐occurring species.more » « less
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Background: The independent evolution of sympatric species pairs of threespine sticklebacks has provided a natural system to explore how divergent ecologies shape mating preferences. Research has shown that both limnetic and benthic females discriminate against heterospecific males, but not against populations of the same species from different lakes, at least when visual cues are available (Rundle et al., 2000). It is known that olfaction is used in species dis- crimination by benthic but not limnetic sticklebacks in one of the species pairs (Rafferty and Boughman, 2006), but differences across populations are unknown. Hypotheses: Females from benthic habitats make use of olfactory cues to distinguish between species but not lakes of potential mates. Limnetic females will not show preferences for males of different species or lakes when limited to only olfactory cues. Organisms: Benthic and limnetic populations of threespine stickleback (Gasterosteus aculeatus) from Paxton and Priest Lakes, British Columbia. Methods: We exposed gravid females from each population to chemical stimuli from nesting males in a Y-maze, and recorded which stimulus a female chose and how much time was taken to make a decision. Results: We did not find significant differences between female populations in the preference for conspecific over heterospecific male odours. There was also no preference for odours of males from the same or a different lake. In all populations of females, the preference for male odours of different lakes differed between the two species of male odours: benthic male odours from a different lake were selected over limnetic male odours. The amount of time taken to make a decision differed between female populations, but only when benthic females ultimately chose a limnetic male odour over a benthic one. Conclusions: The preference for conspecific over heterospecific odours, although not strong, may still contribute to reproductive isolation in sympatric sticklebacks, particularly through interactions with other senses and environmental properties.more » « less
