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Life at the edge: local adaptation and northern range limit for an estuarine sea slug

Life at the edge: local adaptation and northern range limit for an estuarine sea slug. Hanna Koch Dr. Patrick Krug California State University, Los Angeles. Significance of Studying Range Limits.  Fo r basic science, range limits are fundamental to ecology and evolutionary biology:

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Life at the edge: local adaptation and northern range limit for an estuarine sea slug

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  1. Life at the edge:local adaptation and northern range limit for an estuarine sea slug Hanna Koch Dr. Patrick Krug California State University, Los Angeles

  2. Significance of Studying Range Limits  For basic science, range limits are fundamental to ecology and evolutionary biology: • Ecology: What sets distributional limits? A) Biotic factors: competitive exclusion B) Abiotic Factors: gradients in temperature, salinity • Evolution: What prevents adaptation to edge conditions? A) Gene flow from range center B) Lack of underlying genetic variation For applied work, understanding the basis of range limits is critical to predict how species will respond to climate change

  3. Intertidal Animals • Model system: • Ideal for range limit studies • Easily tracked along linear shoreline distribution • North & south endpoints • Exposed @ low tide, submerged @ high tide • No subtidal refuge • Exposed to extreme temps & salinities  “salinity” = concentration of salt in seawater

  4. Alderia willowi Algae • Sea slug that lives in estuaries • Live & feed on algae mats on muddy banks of estuaries • Range = Baja California, Mexico  Tomales Bay, CA • Prefers warmer temps, higher salinities

  5. A. willowi - range edge vs. range center • Tomales Bay (stressful): • range edge • more rainfall  lower salinity • Is northern range limit stable? • Los Angeles (optimal): • range center • more stable environment than TB • warmer temps • 4x less precipitation • higher salinity Tomales Bay Range edge LA Range center

  6. Question: Can A. willowi be locally adapted to conditions at the range edge? Theory predicts that immigrants from range center will flood the range edge with mal-adaptive alleles and inhibit adaptation… • Hypotheses: • The range-edge population (TB) is more locally adapted to low salinity stress than range center (LA) • 2. Local adaptation occurs over rainy season • Low salinity tolerance is a genetic, heritable trait & is favored at the range edge (TB)

  7. Methods- measuring low salinity tolerance (time to death)  time to death at 2‰ scored for 20 slugs per collection I’m dead  Normal, live slug Dissolving, dead slug

  8. Results 1: Local adaptation to edge conditions - survival time in continuous 2‰ SW ANOVA: F2,57 = 10.85, P < 0.001 Before winter onset of low salinity stress, slugs from northern range limit survive 2x as long as established range-center population ….evidence for local adaptation to low salinity stress @ range edge!

  9. Results 2: Local adaptation over rainy season - survival time in continuous 2‰ SW • RC:ANOVA: F1,38 = 6.0, P = 0.019 • RE: ANOVA: F1,38 = 244.12, P < 0.0001 • T-TEST INSTEAD • After onset of winter rains & low salinity stress… • RC slugs saw slight increase in survival • Mean survival of RE slugs increased from 3 hrs to 2 days… •  Suggests rapid local adaptation to edge conditions in RE populations

  10. Adaptation to life on the edge? Is increased low salinity tolerance of Tomales slugs due to… a) phenotypic plasticity? - slugs acclimatize to increasing stress b) maternal effects? - moms under stress buffer their young c) adaptive evolution? - low salinity tolerance is heritable trait

  11. Results 3a: Effects of phenotypic plasticity? - survival time in continuous 2‰ SW FIX GRAPH RC: ANOVA: F1,38 = 0.43, P = 0.5177 RE: ANOVA: F1,38 = 9.26, P = 0.0042 • Treatment = 20 slugs exposed to successively lower salinities • 1 hr shock, every 2 days, over 10 days  shocks: 16, 12, 10, 8, 4‰ • Control = 20 slugs kept @ standard conditions: 32‰, 16o C • At end, a time to death experiment @ 2‰ was performed •  @ range center, no indication of acclimatization to low salinity stress •  @ range edge, slight evidence of slugs exhibiting phenotypic plasticity

  12. Results 3b: Maternal effects? A. willowi Control: 32‰ for 6hr (n=24) Treatment: 6‰ for 6hr (n=24) Treatment @ Level of Mother Low Salinity: 10‰ (n=8) Medium Salinity: 12‰ (n=8) High Salinity: 16‰ (n=8) Treatment @ Level of Offspring • After treatment, mothers lay 1 egg mass each • Eggs masses from control and treatment mothers then divided into 3 treatments (10, 12, 16‰) • For each egg mass, kept @ designated salinity, I measured: • Development time • Performance of offspring  If mother’s experience makes a difference, offspring of low-salinity mothers will be more resistant to low salinity themselves egg mass

  13. Maternal Effects - Development Time DT= time from when egg mass was laid until 1st larva leaves egg mass (n=8) C = Control: Offspring from 32‰ mom T = Treatment: Offspring from 6‰ mom C T C T C T larva • Across all 3 salinity levels, NO significant effect of whether the mother experienced low salinity stress or not on the development time of her offspring • Mother’s experience did not have effect on offspring’s ability to tolerate low salinity stress

  14. Maternal Effects - Performance of Offspring • Shock offspring @ 2‰ for 4 hrs, scored % mortality afterwards • 10 largest slugs in each dish of 8 replicates per salinity treatment C = Control: Offspring from 32‰ mom T = Treatment: Offspring from 6‰ mom C T C T  Mother’s experience did not have effect on offspring performance

  15. Results 3c: Adaptive evolution? • - slugs collected @ same time from range edge, center (gen 0) • offspring reared for 2 generations in lab • time to death experiment performed on all 3 generations • superior low salinity tolerance exhibited in TB offspring •  low salinity tolerance is genetically based, i.e. local adaptation

  16. Conclusions •  For basic science, range limits are fundamental to ecology and evolutionary biology: • Ecology: What sets distributional limits? • A. willowi’s northern range limit set @ TB; stable • Set by abiotic factor: salinity • Evolution: What inhibits adaptation to edge conditions? • Gradients in salinity drive variations in local adaptation for A. willowi across range • @ range center, LA: natural selection on low S tolerance is relaxed • Slight local adaptation, only seen over rainy season • @ range edge, TB: strong selection on low S tolerance • Slight effect of phenotypic plasticity • No evidence for maternal effects • Low salinity tolerance conferred to offspring • Strong evidence for adaptive evolution •  Can A. willowi be locally adapted to range edge conditions? YES!

  17. Thank You • The Krug Lab: Dr. Patrick Krug, Dr. Jann Vendetti, Betsy Shimer, Dominique Gordon, Matthew Garchow, Angela Llaban, Julia Vo, Diane Rico, John Martin, Zar Phyo

  18. Methods- measuring low salinity tolerance (time to death) Vital Staining  time to death at 2‰ was scored for 20 slugs per collection 2 ‰ SW Normal slug I’m alive!  I’m dead  I’m REALLY dead

  19. Maternal Effects - Hatching Success HS = # of developed embryos (that leave the egg mass) vs. # of undeveloped embryos (that don’t) C = Control: Offspring from 32‰ mom T = Treatment: Offspring from 6‰ mom C T C T C T • Across all 3 salinity levels, NO significant effect of whether mother experiences low salinity stress or not on the # of embryos that fully develop & hatch out vs. the # of undeveloped ones • Mother’s experience did not have effect on offspring’s ability to tolerate low salinity stress

  20. Dynamic Range Boundary- Ranges consistently overlap between SF Bay and Bodega Harbor Prefers cooler temps, lower salinities modesta Bodega Harbor Hog Island south Tomales willowi Mill Valley Prefers warmer temps, higher salinities Bolinas lagoon - monitored at 5 sites from 2003-2011

  21. Rainfall correlates with range limits  Bodega receives the most rainfall (modesta advantage)  Tomales consistently gets the least rain (willowiadvantage)

  22. Temperature and range limits max daily temp (oC)  Bodega, Mill Valley consistently colder than Tomales sites

  23. Local Adaptation Selection for low salinity tolerance Selection for high thermal tolerance Migration (gene flow) Env. 1 - Los Angeles Env. 2 – San Fran • Natural selection produces adaptation, but: • Slxn doesn’t always favor same traits in every habitat • Animals don’t always stay in one place • Adaptation results from selection on a heritable trait • Gene flow opposes adaptation

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