Local adaptation in Diopatra-2016

A research effort produced by the Fall 2016 Graduate-level Marine Invertebrate Zoology Course (College of Charleston) 

Report by: Erik Andersson, Nicole Enright, Ben Flanagan, Kevin Mack

Project conceived by: Dr. Erik Sotka 

Special thanks to: Baylye Boxall, Jefferson Canann, Lorenzo Fruscella, Elizabeth Gugliotti, Katie Harper, Zac Lane, Rachel Leads, Lena Pound, Elizabeth Underwood

                                                     Photo credit: South Carolina Department of Natural Resouces

Background

Question: Is there evidence of local adaptation to mudflat tidal zones in the tube-dwelling worm Diopatra cuprea

Environmental conditions vary between any two habitats therefore the selective forces acting on local populations can lead to population environment matching or local adaptation. Adaptation studies at large typically investigate local adaptation because the previous environmental conditions leading any adapted population are near impossible to recreate.  Local adaptation arises through continued natural selection at a local scale when gene flow is high, but when gene flow is low, divergence between two populations may be due to other factors outside of adaptation. Because gene flow works to homogenize connected populations, strong selective forces leading to local adaptation are required to counteract gene flow. Thus, detecting local adaptation can be achieved by studying population performance across native and foreign environments (summarized from Kawecki and Ebert 2004).

The onuphid polychaete worm, Diopatra cuprea (Bosc), is commonly found in intertidal mud flats along the Atlantic coast of the North America ranging from north of Cape Cod to south of Florida (Mangum et al. 1968). This species of worm constructs a mucous tube that typically extends vertically down into the substratum 50 to 60 cm, with an exposed portion of the tube (the tube cap) extending anywhere from 1 to 6 cm above the substrate (Mangum et al. 1968; Myers 1972). These worms actively decorate their tube caps with shell fragments, macroalgae, and other debris in order to provide tube structure and strength (Myers 1972), shelter from predators (Brenchley 1976), and food supply (Mangum et al. 1968). The creation and decoration of these tubes results in a modification of the soft sediment habitat that the worms inhabit, providing areas for macroalgae attachment and thereby habitat for algae-associated invertebrates (Thomsen and McGlathery 2005).

D. cuprea inhabit both the high and low intertidal zones, which are very different environments within the mudflat. It is thought that the pressures in the upper intertidal zone are driven by abiotic factors such as desiccation, sedimentation, and temperature fluctuation. In contrast, it is thought that the pressures in the lower intertidal zone are driven by biotic factors such as predation and parasite loads. It is uncertain whether these worms are locally adapted to the intertidal zone that they inhabit, or if they are exhibiting phenotypic plasticity. Here we perform a transplant experiment of D. cuprea to evaluate local adaptation of the worms to the different intertidal zones (high intertidal zone or low intertidal zone), while utilizing a common garden before out-planting to limit effects of phenotypic plasticity. Survival and fitness measurements are used to assess the worms' ability to inhabit both environments. 

Methods

Our field site behind MRRI on the Ft. Johnson campus was selected due to the presence of Diopatra cuprea, large intertidal area, and ease of access. Two worm collections were conducted, one in the high intertidal (+0.25m above mean low tide) and another in the low intertidal (-0.25m below mean low tide). Worms, and tubes when possible, were collected haphazardly from each tidal height, stripped of Gracilaria decoration, and placed into closed bottom falcon tubes to facilitate transplantation. Worms were allowed to acclimate in the Grice wet lab for a period of 2 to 4 weeks where they were fed intermediately.

Following this acclimation period, two 30 m transects were established at our field site, one in the high intertidal (+0.25m above mean low tide) and another in the low intertidal (-0.25m below mean low tide) (Figure 1). Along each transect, falcon tubes containing live worms were placed at each meter, alternating by intertidal zone of origin. Each transect contained an equal number of control tubes (i.e. worms collected from and outplanted into the same intertidal zone), and treatment tubes (i.e. worms collected from one intertidal zone and outplanted into the other). Falcon tubes were buried to be approximately level with mudflat, leaving a portion of the worm tube exposed above the surface. Worms remained deployed for 2 months before being re-collected and assessed for survival (Figure 2 and Figure 3). During this deployment time, hurricane Mathew disturbed the site. Following re-collection, overall survival was determined for each control and treatment. In addition, we measured tube height above sediment, wet weight of associated/decorated Gracilaria, and worm dry mass as indicators of fitness. For each factor, comparisons were made between intertidal habitat of origin, outplant habitat, and interactions using two-way ANOVA in R.  

Figure 1. Ariel view of D. cuprea outplant locations on the mudflat behind MRRI on the Ft. Johnson campus. The red box indicates the high intertidal (+0.25m above mean low tide) outplant location and the blue box indicates the low intertidal outplant location (-0.25m below mean low tide).

Figure 2. The high intertidal transect after the D. cuprea Falcon tubes had been recovered after being in the field for 2 months. Photo credit: Erik Andersson

Figure 3. The recovered D. cuprea Falcon tubes, before being assessed for survival and other measures of fitness. Photo credit: Erik Andersson

Results and Discussion

No evidence of local adaptation to mudflat habitat was found in D. cuprea, however differences in survival (Figure 4) were detected between the two control treatments (p = 0.035) indicating a lower survival rate in the low intertidal zone compared to the high intertidal. Survival in worms outplanted from low to high, or from high to low did not differ from those that remained in their origin habitats. All worms collected from the high intertidal, that were still present following disturbance, survived. Worms collected from the low intertidal, and outplanted back into that location had a 50% (± 15%) survival rate. Worms from the low intertidal, and outplanted into the high intertidal had a 70% (± 18%) survival rate.

As a proxy of fitness, worm tube height and mass were measured. Differences in worm tube height were detected, with a significant interaction term (p = 0.018) indicating that worms outplanted from high to low intertidal grew significantly longer tubes compared to those that remained in the high intertidal. Tube height did not differ between origin locations, or for those outplanted from low to high.  No significant differences were detected in associated Gracilaria mass or of D. cuprea dry mass (Figure 5).

The nondemonic intrusion of hurricane Mathew likely influenced survival at both locations. Hurricane Matthew made landfall 30 miles north of the study site, causing large in harbor wave disturbance. The wave force likely caused mass destruction and worm vessel loss selectively to the high intertidal outplants rather than the low (Figure 6). Out of 60 worms that were originally outplanted, only 20 were recovered: 11 from the low intertidal (Six of low intertidal origin, five of high intertidal origin) and 9 from the high intertidal (four of high intertidal origin, five of low intertidal origin). We attribute the loss of more individuals in the high intertidal to wave action from Matthew. Additionally, the high intertidal outplants some individuals were protected by an oyster reef recovery project which in turn may have influenced their subsequent survival. Additional work outplanting D. cuprea in more areas, as well as during hurricane offseason will further shed light onto local adaptation in this species.

Figure 4. Survival frequency of the recovered Diopatra cuprea as a function of outplant location. Blue points indicate worms originally collected from the high intertidal zone, red points indicate worms originally collected from the low intertidal zone. All worms that were originally collected from the high intertidal zonesurvived (n=9).

Figure 5. Dry mass of recovered Diopatra cuprea worms as a function of outplant location. Blue points indicate worms originally collected from the high intertidal zone, red points indicate worms originally collected from the low intertidal zone.

Figure 6. Frequency of Falcon tubes unable to be recovered, as a function of outplant location.

Bibliography and Resources

Brenchley G. A. (1976) Predator detection and avoidance: ornamentation of tube-caps of Diopatra spp. (Polychaeta: Onuphidae). Marine Biology 38(2):179-188.

Mangum C. P., Santos S. L. and Rhodes W. R. (1968) Distribution and feeding in the onuphid polychaete, Diopatra cuprea (Bosc). Marine Biology 2(1):33-40.

Myers A. C. (1972) Tube-word-sediment relationships of Diopatra cuprea (Polychaeta: Onuphidae). Marine Biology 17(4): 350-356.

Thomsen M. S. and McGlathery K. (2005) Facilitation of maroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuarine, Coastal and Shelf Science 62:63-73.