What is genetic rescue and what is its role in conservation??
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1 What is genetic rescue and what is its role in conservation?? R. Frankham Macquarie University & Australian Museum Sydney, Australia
2 What is genetic rescue?
3 What is genetic rescue? Reversal of inbreeding and improvement of reproductive fitness from gene flow into inbred populations (heterosis/hybrid vigour) Recovery of ability to evolve due to gene flow into populations with low genetic diversity (evolutionary rescue)
4 What is the problem? Innumerable species have fragmented distributions Population Size OK AR TN KY SC NC VA Approx. 600 MS AL TX GA LA 0.10 FL H N
5 What are the genetic consequences of fragmented distributions? If there is no gene flow between fragments Inbreeding Loss of genetic diversity Reduced reproductive fitness Reduced ability to evolve Elevated extinction risks
6 What is the remedy? Re-establish gene flow (genetic rescue) Reduce inbreeding Restore genetic diversity Improves reproductive fitness Reduced ability to evolve Reduce extinction risk
7 How often is the remedy used? Very rarely being done know only ~ 30 cases worldwide for thr/near thr pops animals & plants Estimate that 1.4m pop fragments of thr sp would benefit from gene flow
8 Why are there so few genetic rescue attempts? 1. Fears about outbreeding depression 2. Lack of clear overview of effects 3. Causal links between G divergence and low GD 4. Overly stringent guidelines 5. Concerns about maintaining genetic purity 6. Costs 7. Risks of disease transfer 8. Regulatory barriers 8
9 What fitness effects have been reported on outcrossing? Often beneficial, some harmful (OD) Edmands (2007) variable McClelland & Naish (2007) fish F , F [SD units] (CI to +0.57), (CI 0.41 to +0.74) Whitlock et al. (2013) animals & plants F %, F 2-8.8% (CI -2.1 to +5.4) (CI -14 to -0.25)
10 Those papers don t reflect the conservation context Only contemplate genetic rescue for isolated inbred population fragments with low genetic diversity Avoid crosses with a high risk of OD Consequently, I did a meta-analysis that reflected the conservation context
11 Meta-analysis aims Evaluate genetic rescue effects in a conservation context Does outcrossing improve the reproductive fitness of small isolated inbred populations where risk of OD is low? How consistently are the effects? How large are the effects? What variables affect the magnitude? Do benefits persist across generations?
12 Data screen in meta-analysis Inbred pop + outcrossed pop Fitness data Low risk of outbreeding depression (Frankham et al. 2011) Same species/sub-species No fixed chromosomal diffs Adapted to similar environments Gene flow within last 500 yrs Excluded selected domestic species
13 Data mining yielded 156 fitness comparisons (going back to Darwin 1876) Involving 77 taxa (18 inverts, 15 verts & 44 plants)
14 Effect size for fitness ( GR) % change in fitness = 100 (outcrossed inbred) inbred
15 How consistent is GR? Data: 145 +: 2 =: 9 (156) 92.9% beneficial*** Highly consistently beneficial effects Screen against OD effective 15
16 What about the exceptions? All mildly harmful 14% 8/9 likely chance (low power, etc) 1 OD: selfing nematode: low ID & G rescue expected & elevated risk of OD 16
17 How large are GR effects? composite fitness in outbreeding species Data: 67 cf Median 84%*** (range -14%- ) Mean 116% (CI 80%; 158%) Wild 151%: captive 51% (likely underestimates)
18 Magnitude of genetic rescue effects for fitness Taxon GR (%) Trait ΔF Breeding Vertebrates African lion 347 # cubs weaned/female NA O system Bighorn sheep 331 female annual reproductive 0.25 O success Desert topminnow fish 7500 total fitness NA O European tree frog 15 tadpole body mass 0.15 O Florida panther 169 composite fitness 0.58 O Greater prairie chicken 26 hatching success 0.10 O Gray wolf (Europe) 23 annual population growth 0.14 O South Island robin 679 reproductive recruitment/egg 0.21 O Swedish adder 233 male recruitment success 0.75 O Invertebrates Glanville fritillary butterfly 211 egg hatching rate 0.41 O Mysid shrimp 318 net increase in N 0.31 O Plants Florida ziziphus fertilization success NA SI Italian ryegrass 43 flowering heads/plant 0.42 SI Jellyfish tree 151 composite fitness 0.31 SI Partridge pea 73 total fitness 0.06 O Small scabious 114 composite fitness 0.15 O Water hyacinth 118 # flowers 0.97 O
19 Accords with fitness data in domestic animals and plants Maize 190% outcrossing Sorghum 100% mainly selfing Layers 22% Cotton 48% selfer Wheat 29% selfer Barley 32% selfer Tomato 45% selfer Swine 72%
20 What variables affect the magnitude? Variables determining ID (opposite sign) Stressful > benign env Inbreeding (ΔF m & ΔF z ) Br system (outcrossing > selfing) Immigrants outbred > inbred (ploidy) Major taxa ns Generation
21 Variables affecting the magnitude of GR (Frankham 2015) Variable Median GR (%) n Mating system Outbreeding > selfing 133 Outbreeding 78.8*** Selfing or mixed mating 16.5 Immigrants Outbred > Inbred 120 Outbred 113.6*** Inbred 51.9 Major taxa (all data) 133 Invertebrates 58.4 ns Vertebrates 94.2 Plants 59.1
22 Do benefits of gene flow persist across generations?
23 Do benefits of gene flow persist (outbreeders)? Effects F 1 F 2 F 3 Beneficial Reduction in inbreeding ( F) - zygotic effects Maximal Stable at ~ ½-¾ F 1 Stable at ~ ½-¾ F 1 - maternal effects Nil Maximal Stable at ~ ½-¾ F 1 Harmful Differential adaptation (additive) - zygotic effects Worst ~ ½ F 1 ~ ½ F 1 - maternal effects Nil Worst ~ ½ F 2 Fixed chromosomal differences: ploidy - Zygotes & maternal Nil (soma) Present* Present* : translocations, inversions and centric fusion - Zygotes & maternal Nil (soma) Worst ~ ½ F 2 Coadapted gene complexes (worsens with generations) Nil Present Worse - Zygotes - maternal Nil Nil/minimal Present 23
24 Persistence of genetic rescue benefits with selfing GR for fitness not persist in selfing species A 1 A 1 x A 2 A 2 A 1 A 2 and the heterozygosity halves in each subsequent generations of selfing Persist less in mixed-mating species than random-mating ones (33-89%)
25 Benefits in F 1, F 2 and F 3 (and later) generations (Frankham 2016) Generation % beneficial n Fitness median benefit F1 90.5*** 95 42%*** 39 F *** 13 84%* 5 F3 and later 94.1*** 17 86%*** 14 n 25
26 But what of persistence of GR beyond F3 in outbreeders? Bijlsma et al. (2010) 26
27 Benefits persist across generations for outcrossing species 27
28 What about the ability to evolve (evolutionary rescue)? Rescued Not
29 Evolutionary rescue for fitness benefit/g Consistency: 6: 0* beneficial Median benefit 22.4%/G Mean 37.6% % Non-fitness traits 35: 4*** beneficial 29
30 Evolutionary rescue increases with heterozygosity
31 Genetic rescue: conclusions 1. Highly consistent benefits of outcrossing on fitness & evol potential 2. OD screen highly effective 3. Fitness benefits large (wild 151%) 4. Benefits = f (environment, ΔF m, ΔF z, br system, & immigrants outbr v inbr) 5. Benefits persisted over generations for outbrs
32 Recommend GR for isolated inbred pop fragments of outx sp, when proposed cross has a low risk of OD, & predicted benefits justify the costs.
33 Genetic Management of Fragmented Animal and Plant Populations Frankham, Ballou, Ralls, Eldridge, Dudash, Fenster, Lacy & Sunnucks Oxford University Press
34 How serious a problem is inbreeding depression? Common name Genus and ID species % Red deer Cervus elaphus 99 Collared Ficedula albicollis 94 a flycatcher Great tit Parus major 55 Song sparrow Melospiza melodia 79 Takahe Porphyrio 88 hochstetteri Deerhorn clarkia Clarkia pulchella 100 a Rose pink plant Sabatia angularis 38 a Wild radish Raphanus sativus 58 a a No maternal component 34
35 Proportion surviving Inbreeding and extinction Lab studies Field studies Simulations FS F 400 African lion 300 N
36 Estimation number of thr populations that would potentially benefit from gene flow # benefiting = # species x P (thr) x P (frag & isol) x av # fragments x P (inbred) = 8.7m x 0.2 x 0.4 x 10 x 0.2 = 1.4m
37 Causal links between genetic divergence & loss GD Theory F ST 2 p 1 pq H H S T Empirical Coleman et al. (2013) 37
38 Genetic management of fragmented populations is one of the most important, largely unaddressed issues in all of conservation biology Genetic rescue is a crucial part of that
39 A paradigm shift 39
40 F maternal lags F zygote by 1 gen Generation F Litter size Maternal Zygotic in mice Outbred Full-sib F1 (inb x inb) Inbreeding depression = 2.43 F (6.7) F1 x diff F Genetic rescue = 2.78
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