Speciation Mechanisms

Although some flies have attained a scientific spotlight in the field of speciation, such as the omnipresent Drosophila genus to the confusing Rhagoletis pomonella group, most other Dipterans rarely serve as model organisms. Such is the case of Strauzia, which spends its adult life hanging to sunflowers and allies, while mining in the stems of its host plants during its larval life (Stoltzfus, 1988). Earlier research into the group focused largely on taxonomy and host plant associations, while Strauzia as a model of speciation has largely been unrecognized until recently with the work of the Forbes lab. Based on the research of the past decade, it is likely that Strauzia was formed through sympatric ecological speciation, based around host shifts in the past and prezygotic barriers to gene flow.

The original framework of Strauzia consisted of a single variable, polyphagous species (Loew, 1873). One of the signs that this idea was inadequate for describing the natural state of Strauzia was the regular differences between “varieties”, even those on the same plant. The majority of these variants were elevated to species level in the 1980’s (Steyskal, 1986; Stoltzfus, 1988), and other unrecognized species were described, often being closely allied morphologically with Strauzia longipennis. Notably, so closely related were their morphologies that some of these moves from variant to species level were not supported by future researchers until more studies were done on the level of differentiation between the groups (Foote et al., 1993). Further complicating this research was that it appeared that multiple species/variants of Strauzia existed on the same species of sunflower, which caused confusion on whether they were a single polymorphic species or separate species who all somehow ended up on the same plant over evolution (Stoltzfus, 1988; Axen et al., 2010). Indeed, until a year ago, the barriers between these species/variants remained elusive, with different genetic “races” and haplotypes being found but no clear division that mapped onto their morphological traits (Forbes et al., 2012; Hippee et al., 2016).

Wing patterns 38-54 from Stoltzfus, 1988; figures enclosed in red boxes were formerly included under Strauzia longipennis.

Figure 1 from Forbes et al., 2017.

At the core of studying speciation within Strauzia are the concepts of ecological speciation and host shifting. No species forms under an environmental vacuum of course, but ecological speciation of phytophagous insects is recognized as speciation is a consequence of a species with its environment and selection from the environment itself (Matsubayashi et al., 2010). This is particularly notable for phytophagous insects, as the environment can be viewed through the lens of the host plant, or whatever plant is used for a given state of life, and how tied they are to that plant. Most of the species of Strauzia are currently recognized as being monophagous or narrowly oligophagous (Hippee et al., 2020), so understanding how a species came to use a plant is critical. Host shifts are the event where an insect changes its host plant that is used for the life cycle, and then continues to use this plant in future generations. The above figure from Forbes et al., 2017, illustrates the three ways a host shift may be involved with speciation. With the first category where a host shift initiated speciation, there were no reproductively isolated populations before the host shift occurred, while in the second category where the host shift only contributed to speciation, the populations had some level of gene flow and thus incomplete isolation (Forbes et al., 2017). There is also the possibility that a host shift occurred after speciation. It is difficult to prove which of these two is the case in any given system as evidence that no isolating barriers existed prior to the host shift are needed, which would mean the host shift needs to happen during the time of scientific observation. An example of this occurring within Tephritidae is with Rhagoletis pomonella, where the host shift happened within the last 200 years and was documented by scientists of that era, and that the host shift is associated with different host races (Michel et al., 2010).

Figure 1 from Hippee et al., 2020.

Unfortunately, all speciation within Strauzia has been estimated to have occurred between 0.6 to 0.1 million years ago (Hippee et al., 2020), so we can’t rely on observational data of a host shift for a decision on which of the three scenarios from Forbes et al., 2017 is most applicable. However, by using phylogenetic techniques, the presence of host shifts in the evolutionary history of a group can be revealed. Within Strauzia, it was found that fly species using the same sunflower species such as Helianthus tuberosus were actually not each other’s closest relatives (Hippee et al., 2020). What this implies is that host shifts occurred in the past, and that multiple fly species shifted at different points to the same sunflower species, as exampled by the second row in the above figure. To summarize, this would all occur under a system of sympatric ecological speciation.

Figure 5 from Forbes et al., 2012. Only groups I, II, and III were significantly different from each other.

The main studies into barriers to gene flow that exist between different species of Strauzia have focused on temporal differences and female mate choice. The first worker to notice the role temporal differences in life cycles could have in species differentiation was Stoltzfus, who recognized there being three species of Strauzia that used Helianthus tuberosus, but the time when major life cycle events happened were distinct among the three species (Stoltzfus, 1988). This idea laid dormant for a time after its publication, but was picked up again when different members of the S. longipennis complex were collected and sorted into three groups based on genetic markers (Forbes et al., 2012). From this, it was revealed once again that three of the members of this group had significantly different times of peak population across the summer. This finding, where different members of the S. longipennis complex on Helianthus tuberosus had different population peaks, was once again shown to occur yearly over four years of collection (Hippee et al., 2016). As such, it is clear that temporal isolation exists for these related species of Strauzia, which is a prezygotic barrier to gene flow that could have been caused by ecological speciation. The second studied barrier to gene exchange in this study is mate choice, and in all crosses set up, the frequency of conspecific mating was significantly higher than that of interspecific pairs. Interestingly, the effect of mating choice as a potential prezygotic barrier to gene flow was shown to be less strong in these members of the S. longipennis complex on Helianthus tuberosus, but this could imply a stronger role of the allochronic population peaks of these species compared to mate choice. Both of these pre-zygotic barriers to gene flow could have arisen from ecological speciation, especially in the case where the flies adapted to the different life cycles of the plants they use as hosts.

Figure 1 from Hippee et al., 2016.

Continuing off of the mating experiments of Hippee et al., 2016, there is the important existence of sexual dimorphism that has confused past workers in this group. Although it wasn’t recognized in the early works of Strauzia taxonomy, it is now known that in some species, there is strong sexual dimorphism in the wing patterns between male and female members of a given species (Stoltzfus, 1988). Females in particular have wing patterns that are similar to each other between species, while males have more distinctive wing patterns. The above figure shows that the wing pattern for males separate clearly into 4 different groups in a K=4 structure plot, while the females are morphologically cryptic and couldn’t be separated by their wing patterns. This mirrors many other systems in ecological systems where female sexual selection causes a stronger differentiation of secondary sexual characters in males, while females differentiate less (Dale et al., 2015).

On the seemingly cryptic morphology of the wing patterns, there is growing evidence that wing interference patterns (WIPs) are a crucial component of species recognition for flies, and this is another area of potential research (Butterworth et al., 2021). As a pre-zygotic barrier to gene flow, female mate choice could be playing a relatively large role in speciation (Dopman et al., 2010). However, the role that sexual selection plays in speciation within Strauzia has not been studied, but theoretically could be linked with the sympatric host shifting hypothesis. This is because if there is some sort of fitness reduction for hybrids on the same plant, females that prefer conspecific males should have an advantage in passing down their genes, thus creating a system of sexual selection that supports assortative mating of conspecific flies on a given plant.

Figure 2 from Butterworth et al., 2021. Wing interference patterns of Chrysomya (Diptera: Calliphoridae) are shown to be differentiated between both species and sex, much like the wing patterns of Strauzia.

Figure 5 from Forbes et al., 2012.

Although postzygotic barriers to gene flow can sometimes have a lesser sequential strength in the overall scheme of separating populations (Dopman et al., 2009), the rate at which these mechanisms appear in Strauzia, and what role they play in speciation, are not clear from the current literature. For example, multiple studies have shown that mating does occur between different species of Strauzia (Axen et al., 2010; Hippee et al., 2016), but due to the life cycle of Strauzia it has been hitherto impossible to test hybrid fitness. Gametic incompatibility was not tested in the mating trials of Hippee et al., 2016, but theoretically could be in order to examine if that exists as a prezygotic post-mating barrier to gene exchange. Another interesting aspect that has been observed is potential introgression and backcrossing in the evolutionary past. In the above diagram from Forbes et al., 2012, their analysis of three genetic clusters of H. tuberosus using Strauzia implied that 2 events of introgression occurred in the divergence of these groups sometime over their million year evolutionary history. More sampling and analyses could further reveal the potential rate of introgression in Strauzia, which would allow for better accuracy of speciation theories within the genus.

Despite their general anonymity, Strauzia manages to confuse and enrapture the scientists who know of its existence and history, a million years of fluttering around sunflowers in the prairie. At this point, it is almost certain that ecological speciation was a driving force in the differentiation of Strauzia populations, especially due to the close host plant relationship Strauzia flies have, and the evidence of sympatric host shifts in the past. Allochronic separation and mate choice have been shown to act as prezygotic barriers to gene flow, but more research into genetic barriers should be done to better understand the process of hybridization and introgression that appears to have happened in the past.

[iNaturalist Photo 83876528, (c) Daniel Onea, some rights reserved (CC BY-NC)]. Strauzia flies mating.

Works Cited

Axen HJ, Harrison JL, Gammons JR, McNish IG, Blythe LD, Condon MA (2010). Incipient Speciation in Strauzia longipennis (Diptera: Tephritidae): Two Sympatric Mitochondrial DNA Lineages in Eastern Iowa. Ann Entomol Soc Am 103(1):11-19. https://doi.org/10.1093/aesa/103.1.11

Butterworth NJ, White TE, Byrne PG, Wallman JF (2021). Love at first flight: wing interference patterns are species specific and sexually dimorphic in blowflies (Diptera: Calliphoridae). J Evol Biol 34:558-570. https://doi.org/10.1111/jeb.13759

Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M (2015). The effects of life history and sexual selection on male and female plumage colouration. Nature 527:367-370. https://doi.org/10.1038/nature15509

Dopman EB, Robbins PS, Seaman A (2009). Components of Reproductive Isolation Between North American Pheromone Strains of the European Corn Borer. Evolution 64(4):881-902. https://doi.org/10.1111/j.1558-5646.2009.00883.x

Foote RH, Blanc FL, and Norrbom AL (1993). Handbook of the Fruit Flies (Diptera: Tephritidae) of America North of Mexico. Comstock Publishing Associated. xii + 571 p.

Forbes AA, Kelly PH, Middleton KA, Condon MA (2012). Genetically differentiated races and speciation-with-gene-flow in the sunflower maggot, Strauzia longipennis. Evol Ecol 26(6):1017-1032. https://doi.org/10.1007/s10682-012-9622-y

Forbes AA, Devine SN, Hippee AC, Tvedte ES, Ward AKG, Widmayer HA, Wilson CJ (2016). Revisiting the particular role of host shifts in initiating insect speciation. Evolution 71(5):1126-1137. https://doi.org/10.1111/evo.13164

Hippee AC, Elnes ME, Armenta JS, Condon MA, Forbes AA (2016). Divergence before the host shift? Prezygotic reproductive isolation among three varieties of a specialist fly on a single host plant. Ecol Entomol 41:389-399. https://doi.org/10.1111/een.12309

Hippee AC, Beer MA, Bagley RK, Condon MA, Kitchen A, Lisowski EA, Norrbom AL, Forbes AA (2020). Host shifting and host sharing in a genus of specialist flies diversifying alongside their sunflower hosts. J Evol Biol 1–16. https://doi.org/10.1111/jeb.13740

Loew H (1873). Monographs of the Diptera of North America. Part III. Smithson. Misc. Collect. 11 (3 [= pub. 256]). VII+ 351+ XIII p.

Michel AP, Sim S, Powell THQ, Taylor MS, Nosil P, Feder JL (2010). Widespread genomic divergence during sympatric speciation. P Natl Acad Sci USA 107(21):9724-9729. https://doi.org/10.1073/pnas.1000939107

Matsubayashi KW, Ohshima I, Nosil P (2010). Ecological speciation in phytophagous insects. Entomol Exp Appl 134:1-27. https://doi.org/10.1111/j.1570-7458.2009.00916.x

Steyskal GC (1986). Taxonomy of the Adults of the Genus Strauzia Robineau-Desvoidy (Diptera: Tephritidae). Insecta Mundi 1(3): 101-117.

Stoltzfus WB (1988). The Taxonomy and Biology of Strauzia (Diptera: Tephritidae). Journal of the Iowa Academy of Science: JIAS 95(4): 117-126.

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