The Riddle of How Fisheries Influence Genetic Diversity

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ The Riddle o How Fishe ies In luence Gene ic Di e si y © 2023 by he au ho s. Licensee MDPI, Basel, Swi ze land Published e sion Sadle , Daniel E.; Wa s, Phillip C.; Uusi-Heikkilä, Sil a Sadle , D. E., Wa s, P. C., & Uusi-Heikkilä, S. (2023). The Riddle o How Fishe ies In luence Gene ic Di e si y. Fishes, 8(10), A icle 510. h ps://doi.o g/10.3390/ ishes8100510 2023 Ci a ion: Sadle , D.E.; Wa s, P.C.; Uusi-Heikkilä, S. The Riddle o How Fishe ies In luence Gene ic Di e si y. Fishes 2023,8, 510. h ps://doi.o g/ 10.3390/ ishes8100510 Academic Edi o : E ic Halle man Recei ed: 31 Augus 2023 Re ised: 5 Oc obe 2023 Accep ed: 12 Oc obe 2023 Published: 13 Oc obe 2023 Copy igh : © 2023 by he au ho s. Licensee MDPI, Basel, Swi ze land. This a icle is an open access a icle dis ibu ed unde he e ms and condi ions o he C ea i e Commons A ibu ion (CC BY) license (h ps:// c ea i ecommons.o g/licenses/by/ 4.0/). ishes Re iew The Riddle o How Fishe ies In luence Gene ic Di e si y Daniel E. Sadle , Phillip C. Wa s and Sil a Uusi-Heikkilä * Depa men o Biological and En i onmen al Science, Uni e si y o Jy äskylä, 40500 Jy äskylä, Finland; [email p o ec ed] (D.E.S.); [email p o ec ed] (P.C.W.) *Co espondence: [email p o ec ed] Abs ac : O e ishing d i es popula ion decline, which in u n d i es loss o gene ic di e si y. Many s udies p o ide e idence o declines in gene ic di e si y; howe e , con o e sy exis s wi hin he li e a u e, as some s udies show e idence o no change in gene ic di e si y despi e decades o o e ha es ing. The appa en disc epancy in he li e a u e should he e o e be examined o unde s and wha biological and ecological p ocesses a e d i ing he di e ences in esul s. He e, we assess how di e en ac o s con ibu e o ishe ies-induced suscep ibili y o declines in gene ic di e si y by i s ocusing on he di e en oles o gene ic ma ke s. Second, we assess how habi a ype and condi ions con ibu e o loss o gene ic di e si y. Thi d, we assess how li e his o y and physiology a ec s ca chabili y and loss o gene ic di e si y. Finally, we discuss how coinciding abio ic and bio ic ac o s in luence he in ensi y o gene ic loss. We ind a mul i ude o hese ac o s could be in e ac ing o in luence how esul s a e pe cei ed and how in ense he loss o gene ic di e si y can be. Fu u e s udies should ca e ully conside he me hodology o gene ic analysis used, as well as conside a ions o li e his o y and ecology o he a ge species. Keywo ds: gene ic di e si y; ishe ies; conse a ion gene ics; size selec ion; popula ion gene ics Key Con ibu ion: This e iew assesses he impo ance o conside ing mul iple ac o s ha could a ec he ulne abili y o an o e ished popula ion o loss o gene ic di e si y. 1. In oduc ion Fish s ocks a e a c ucial sou ce o li elihood and nu i ion, p o iding 156 million onnes o ood pe annum, ep esen ing some 17% o global animal p o ein consumed [ 1 ]. Howe e , because o a 122% inc ease in ish consump ion along wi h his o ic o e ha es - ing, he pe cen age o ish s ocks ha a e ha es ed sus ainably has educed om 90% o 65.8% om 1990 o 2017 [ 1 ]. O e ishing no only causes conce ns o global ood secu i y, bu also emains a he o e on o he an h opogenic p oblems he aqua ic en i onmen aces, causing se e e popula ion declines and habi a des uc ion [ 2 – 4 ]. Indeed, he mode n consensus is ha despi e he high ecundi y o many ish species (e.g., wi h indi iduals o ce ain species capable o p oducing ens o hund eds o housands o eggs in a spawning e en ), his is no enough o main ain a sus ainable s ock unde in ensi e ha es ing [ 5 ]. Cu en p edic ions sugges ish s ocks may become exhaus ed by 2050 [ 6 , 7 ], which no only esul s in popula ion losses, bu a po en ial loss o s anding gene ic di e si y [ 8 ], leading o localised ecosys em collapse, as al eady expe ienced in places such as he Black Sea [9]. Because ishing mo ali y can be ex emely high and ishe ies a e o en also selec i ely emo ing ce ain pheno ypes om he popula ion (i.e., exposing ish popula ions o di- ec ional selec ion), ishe ies can be expec ed o educe gene ic di e si y in an exploi ed popula ion. Indeed, di ec ional selec ion, o en occu ing h ough size-selec ion a ou ing he smalles indi iduals in a popula ion, will no only ac on pheno ypic ai s (e.g., body size, age a ma u a ion, and ep oduc i e ou pu [ 10 ]), bu also on he associa ed gene ic s uc u e. As such, di ec ional selec ion can ac in andem wi h demog aphic loss o en- hance he loss o gene ic di e si y. Decline in gene ic di e si y can lead o educed adap i e Fishes 2023,8, 510. h ps://doi.o g/10.3390/ ishes8100510 h ps://www.mdpi.com/jou nal/ ishes Fishes 2023,8, 510 2 o 14 po en ial [ 11 , 12 ]. Howe e , he e is some deba e whe he neu al di e si y can be uly ep esen a i e o adap i e po en ial, as he genes de ec ed do no ha e any di ec e ec on popula ion i ness [ 13 ]. Reduc ions in adap i e po en ial can lead o inc eased ulne abili y o u u e an h opogenic s esso s. The educ ion in gene ic di e si y can cause educed pheno ypic a iabili y, which in u n may a ec popula ion iabili y and s abili y [ 14 ]. Indeed, e idence o educed gene ic di e si y in exploi ed ish s ocks has been epo ed by a ious s udies, o example, as an inc ease in inb eeding coe icien o a educ ion in e ec i e popula ion size [8,15,16]. Many s udies ha e ied o assess he e ec o ishing s ess on he gene ic di e si y o ish popula ions wi h mixed esul s, wi h some s udies showing clea declines in gene ic di e si y. Fo example, Hause e al. [ 15 ] showed ha he o e exploi a ion o he New Zealand snappe (Pag us au a us) esul ed in a la ge educ ion in bo h gene ic di e si y (he e ozygosi y and numbe o alleles) and e ec i e popula ion size (N e ). Howe e , Jones e al. [ 17 ] ound highe N e alues han expec ed in he o iginal s udy by inco po a ing a la ge sample size and simula ion-based me hods, hough, despi e his, N e was s ill ound o be lowe in exploi ed popula ions han in non-exploi ed popula ions. In con as , o he s udies ha e ound no signi ican educ ions in gene ic di e si y in o e exploi ed s ocks, such as in A lan ic cod (Gadus mo hua) s ocks [ 5 , 18 – 20 ]. Howe e , s ocks expe iencing ela i ely low ca ch a es, such as mango ilapia (Sa o he odon galilaeus) in he sea o Galilee, show a signi ican loss in gene ic di e si y [ 21 ]. Pinsky and Palumbi [ 8 ] comple ed a comp ehensi e me a-analysis u ilising 140 species, demons a ing an o e all end ha o e ha es esul ed in a decline in gene ic di e si y ac oss ma ine ish species, while some s udies show no appa en gene ic loss when exposed o ishing s ess [ 16 , 22 , 23 ]. I is he e o e impo an o unde s and why some s udies appa en ly demons a e clea e idence o loss o gene ic di e si y when exposed o ishing s ess, whils o he s do no . The possible easons why some s ocks do no exhibi a no able loss o gene ic di e si y appea complex, and he li e a u e emains di ided. The magni ude o mo ali y a es and he in ensi y o di ec ional selec ion de e mine how much ishe ies can e ode gene ic di e si y in a popula ion, alongside ini ial popula ion size, e ugia om ishe ies, and mig a ion a e [ 8 ]. Howe e , he a iance in esul s om he li e a u e sugges s ha many o he ac o s ha in luence gene ic di e si y mus be conside ed. This disc epancy may be a esul o changes in gene ic echnologies esul ing in di e ing esolu ions be ween gene ic ma ke s such as single-nucleo ide polymo phisms (SNPs) and mic osa elli es (e.g., [ 24 ]). Fu he mo e, habi a di e si y may ha e an in luence, o example, due o ac o s such as habi a complexi y ha may a ec ulne abili y o being caugh by ishing gea (i.e., ca chabili y; [ 25 , 26 ]), species me apopula ion s uc u e (which de e mines pa e ns o dispe sal among popula ions), and/o whe he a species’ ange encompasses p o ec ed a eas. Mo eo e , li e his o y and beha iou al ai s can a ec ca chabili y and consequen ly loss o gene ic di e si y [ 27 ]. I is also impo an o no e he e olu iona y his o y o a popula ion, and how di e en species di e in hei ulne abili y o ishe ies s ess based on hei e ol ed se o li e his o y ai s [ 28 ]. Finally, o e ishing is no he only s esso e iden in he aqua ic en i onmen , wi h u he an h opogenic e ec s such as clima e change and habi a loss likely con ibu ing o exace ba ing he loss o gene ic di e si y [25]. In his li e a u e e iew, we will assess how di e en ac o s con ibu e o ishe ies- induced suscep ibili y o educ ions in gene ic di e si y and aim o un a el why disc ep- ancy in popula ion esponses in he li e a u e exis s. Fi s , we ocus on he ole o di e en gene ic ma ke s and me ics used o measu e a iabili y in gene ic di e si y p oduced by he di e en s udies. Second, we conside how habi a ype and condi ions can con ibu e o he ishe ies-induced loss o gene ic di e si y. Thi d, we assess he e ec o li e his o y ai s on ca chabili y and loss o gene ic di e si y, and inally discuss how coinciding ac o s in luence he in ensi y o gene ic loss. Fishes 2023,8, 510 3 o 14 2. Gene ic Ma ke s and Me ics S udies ocusing on de ec ing po en ial ishe ies-induced changes in gene ic di e si y ha e used di e en gene ic ma ke s. One eason why he in e p e a ions o ishe ies’ e ec s on gene ic di e si y a y could be ela ed o he ma ke s oge he wi h he me ics u ilised in hese s udies [ 24 , 29 ]. He e, we e iew he mos common ma ke s used in he s udies and discuss how and why hey migh p oduce di e en esul s. 2.1. AFLPs Pionee ing s udies on gene ic di e si y u ilised DNA inge p in ing in he o m o ampli ied agmen leng h polymo phisms (AFLPs). This echnique u ilises es ic ion enzymes o diges DNA, c ea ing es ic ion agmen s which a e hen ampli ied, allowing he de ec ion o DNA polymo phisms [ 30 ]. AFLPs we e popula as hey we e an easy and cheap way o ob ain high-quali y genomic da a [ 31 , 32 ], and hey ha e been used in gene ic di e si y s udies in ishe ies esea ch. Fo example, Wan e al. [ 33 ], used DNA inge p in ing o assess changes in he gene ic di e si y o Dab y’s s u geon (Acipense dab yanus) om 1958 o 1999 a e la ge-scale declines, pa ly due o o e ishing, and showed a signi ican educ ion in gene ic di e si y. AFLPs a e obus , highly ep oduceable, and can be in o ma i e in la ge numbe s [ 31 ]. Howe e , AFLPs a e o en di icul o analyse, equi ing high-quali y, highly pu e DNA, and as a dominan ma ke hey do no de ec he e ozygo es. Hence, he echnique has been mos ly eplaced by o he echniques [ 31 , 34 ]. 2.2. Mi ochond ial DNA Mi ochond ial DNA (m DNA) is being used mo e o en o assess changes in gene ic di e si y compa ed o AFLPs [ 21 , 35 – 38 ]. This echnique u ilises cy och ome c oxidase subuni I (COI) and he D-loop sec ion o m DNA. In e es ingly, s udies using m DNA ubiqui ously show a decline in gene ic di e si y caused by ishe ies [ 37 – 39 ]. Fo example, Johnson e al. [ 37 ] (2018) showed ha di e si y signi ican ly dec eased a e his o ical ha - es ing o Chinook salmon (Onco hynchus shawy scha). Mo eo e , in a s udy on swo d ish (Xiphias gladius) in he Medi e anean, a loss o haplo ype di e si y and N e was de ec ed in emales, which a e la ge and po en ially mo e hea ily a ge ed by ishe ies [ 38 ]. m DNA may be mo e sensi i e o gene ic loss han genomic DNA; howe e , m DNA exhibi s a much slowe a e o e olu ion han genomic DNA due o i s highly conse a i e na u e [40–42] . The e o e, m DNA is conside ed less use ul o examining ecen changes in gene ic di e si y. Howe e , when assessing his o ical DNA alongside genomic DNA, m DNA is a sui able choice o ma ke . Fo example, B o oski e al. [ 21 ] used a combina ion o mic osa elli es and m DNA o show ha mango ilapia expe ienced a bo leneck e en dec easing gene ic di e si y, possibly due o a combina ion o o e ishing and decline in en i onmen al condi ions. 2.3. Mic osa elli es Mic osa elli es emain he gene ic ma ke o choice in he majo i y o s udies analysing gene ic di e si y in exploi ed popula ions [ 43 – 45 ]. This is due o hei inhe en high polymo phism, apid mu a ion a e, and ela i ely low cos [ 43 , 46 ]. Ea ly s udies on gene ic di e si y ypically used a small numbe o mic osa elli es, e.g., [ 47 , 48 ]. This may ha e masked disc e e changes in di e si y, as i has been demons a ed ha s udies conduc ed wi h ewe han 10 mic osa elli e loci ha e low s a is ical powe o de ec changes in gene ic di e si y [ 8 , 49 – 51 ]. Only a mino i y o s udies ha e used mo e han 10 loci o de ec changes a e an o e ha es ing e en ; hese include a lake ou (Sal elinus namaycush) s udy wi h 18 loci [ 52 ], a s udy on dusky kob (A gy osomus japanicus) wi h 18 loci [ 53 ], and a s udy on Eu opean eel (Anguilla anguilla) u ilizing 22 loci [54]. Despi e being a popula choice o gene ic ma ke , mic osa elli es ha e one majo disad an age. They a e neu al ma ke s, meaning hey occu in non-coding egions in he genome as opposed o o he echniques like SNPs ha occu in coding egions. The e o e, whils hey can be used o es ima e changes in, o example, e ec i e popula ion size (N e ), hey canno de ec loss o adap i e gene ic di e si y as unc ional ma ke s can [ 55 ]. Fishes 2023,8, 510 4 o 14 Ins ead o using mic osa elli es alone, a mo e op imal solu ion could be a combina ion o mic osa elli es, SNPs, and educed ep esen a ion lib a y (RRL) sequencing [24,29]. 2.4. SNPs SNPs a e cu en ly he eme ging gene ic ma ke o s udies on ishe ies’ e ec s on gene ic di e si y [ 56 – 58 ]. SNPs a e a po en ial eplacemen o mic osa elli es as hey o e g ea e powe o de ec ion o gene ic change han small numbe s o mic osa elli e ma k- e s [ 59 ]. SNPs can be u ilised in a a ie y o ways om using a SNP a ay ac oss he genome (e.g., [ 10 ]) o sequencing me hods using a la ge numbe o SNPs such as in Res ic ion Si e Associa ed sequencing (RADseq; e.g., [ 60 ]), RNA sequencing [ 61 ], and whole-genome sequencing [ 58 ]. Fu he mo e, SNPs can be used as diagnos ic ma ke s, which can explain a la ge amoun o a ia ion in one ai . Ba son e al. [ 62 ] used 200,000 SNPs and ound a la ge e ec locus (VGLL3) esponsible o age a ma u a ion in A lan ic salmon (Salmo sala ). They ocused on his pa icula locus and showed ha i was esponsible o 39% o he pheno ypic a ia ion obse ed in he popula ion; changes in he allele equency o his loci can help de ec e olu iona y changes in age and size a ma u a ion in exploi ed salmon popula ions, in o ming managemen s a egies. D’Aloia e al. [ 24 ] compa ed h ee gene ic ma ke s, namely mic osa elli es, non- epe i i e nuclea loci, and SNPs, o de e mine how each ma ke ype could al e he gene ic me ics p oduced in a popula ion gene ics s udy. They sequenced he DNA o a ee ish (Elacan inus lo i) using 2418 SNPs, 89 mic osa elli es, and 57 non- epe i i e nuclea loci. The SNPs showed highe F ST alues ( he amoun o gene ic a iance wi hin a sub- popula ion compa ed o gene ic a iance wi hin he en i e popula ion; [ 63 ]) han he o he ma ke s and showed g ea e esolu ion o gene ic s uc u e, allowing o mo e ine-scaled analysis. Howe e , when compa ing o he di e si y me ics, such as expec ed he e ozygos- i y, obse ed he e ozygosi y, and allele ichness, alues we e highes in he mic osa elli e da a. I is also impo an o no e ha mic osa elli e and non- epe i i e nuclea loci a e cheape op ions, and a la ge numbe o hem may be mo e cos -e ec i e han SNPs [ 29 , 60 ]. Despi e his, mode n sequencing me hods u ilizing a high numbe o SNPs may sol e some o he p io men ioned p oblems, as shown by mo e ecen s udies [ 23 , 56 – 58 , 64 ]. Ye , mixed esul s s ill p eside wi hin hose s udies u ilising SNPs, which may be explained by he low numbe o SNPs used. The kildsen e al. [ 58 ] u ilised o e wo million SNPs and showed a signi ican educ ion in gene ic di e si y (nucleo ide di e si y and polymo phism %) in an expe imen ally ha es ed ish popula ion. In con as , Pinsky e al. [ 65 ] used app oxima ely 350,000 SNPs and demons a ed no change in gene ic di e si y (genome-wide di e si y) despi e la ge-scale ha es ing o cod. Sadle e al. (Unpublished), on he o he hand, u ilized almos 3.5 million SNPs and showed a dec ease in gene ic di e si y (he e ozygosi y, nucleo ide di e si y, and N e ) in size-selec i ely ha es ed expe imen al zeb a ish (Danio e io) popula ions. When di e en gene ic ma ke s a e u ilised, di e en me ics a e epo ed, and hese a e no always compa able. Fo example, allele ichness and di e si y a e mo e p one o educ ions in popula ion size han he e ozygosi y [ 14 , 66 ]. The e o e, i a s udy only u ilises he e ozygosi y as a me ic (e.g., [ 48 ]), o he aspec s o gene ic di e si y change could be o e looked. C ucially, s udies should conside ca e ully he implica ions o me hodology used, aiming o he mos e icien , low-cos me hod ha a ge s adap i e loci. 3. Habi a Type 3.1. F eshwa e s. Sal wa e Habi a ype has a signi ican e ec on he ulne abili y o aqua ic species o ex- ploi a ion, he mos ob ious di ide being he di e ence be ween eshwa e and sal wa e habi a s, oge he wi h he in e media e b ackish en i onmen . Despi e he la ge di e ence in habi a size o global aqua ic en i onmen s (0.5% accessible eshwa e and 96.5% sal - wa e ; [ 67 ]) he di e si y o ish is e y simila , wi h app oxima ely 15,000 ac inop e ygian ish species p e alen in bo h ecosys ems [ 68 , 69 ]. The high species di e si y obse ed in Fishes 2023,8, 510 5 o 14 he eshwa e ealm likely o igina es om la ge deg ees o habi a agmen a ion h ough di e en ia ed i e s and isola ed lake and pond sys ems, allowing o g ea e oppo uni y o adap i e di e gence o ake place compa ed o he compa a i ely ubiqui ous habi a o he oceans [68]. S uc u ally, ma ine and eshwa e sys ems a e e y di e en , wi h g ea e habi a connec i i y in he ma ine en i onmen due o he huge expanse o a ailable habi a space. Indeed, gene ically, ma ine ish exhibi less gene ic s uc u e han eshwa e species [ 20 , 70 ]. I may be p esumed ha eshwa e habi a s a e mo e p one o gene ic loss due o he e being ewe e ugia om ishe ies and lowe connec i i y es ic ing mig a ion. Despi e his, mos s udies ocus on ma ine species due o hei inhe en comme cial impo ance, wi h a cap u e o 84 million onnes compa ed o 12 million onnes in eshwa e ishe ies in 2018 [ 1 ]. Howe e , eshwa e en i onmen s expe ience high ishing p essu e [ 71 ], ye less is known abou how ishe ies a ec hei gene ic di e si y. S udies ha ocus on eshwa e sys ems, show a g ea e decline in gene ic di e si y compa ed wi h s udies ocusing on ma ine habi a s (Figu e 1a; Table S1). F eshwa e sys ems may he e o e be mo e p one o loss o gene ic di e si y when exposed o ishe ies s ess. Fishes 2023, 8, 510 5 o 15 di e ence in habi a size o global aqua ic en i onmen s (0.5% accessible eshwa e and 96.5% sal wa e ; [67]) he di e si y o ish is e y simila , wi h app oxima ely 15,000 ac- inop e ygian ish species p e alen in bo h ecosys ems [68,69]. The high species di e si y obse ed in he eshwa e ealm likely o igina es om la ge deg ees o habi a agmen- a ion h ough di e en ia ed i e s and isola ed lake and pond sys ems, allowing o g ea e oppo uni y o adap i e di e gence o ake place compa ed o he compa a i ely ubiqui ous habi a o he oceans [68]. S uc u ally, ma ine and eshwa e sys ems a e e y di e en , wi h g ea e habi a connec i i y in he ma ine en i onmen due o he huge expanse o a ailable habi a space. Indeed, gene ically, ma ine ish exhibi less gene ic s uc u e han eshwa e spe- cies [20,70]. I may be p esumed ha eshwa e habi a s a e mo e p one o gene ic loss due o he e being ewe e ugia om ishe ies and lowe connec i i y es ic ing mig a- ion. Despi e his, mos s udies ocus on ma ine species due o hei inhe en comme cial impo ance, wi h a cap u e o 84 million onnes compa ed o 12 million onnes in esh- wa e ishe ies in 2018 [1]. Howe e , eshwa e en i onmen s expe ience high ishing p essu e [71], ye less is known abou how ishe ies a ec hei gene ic di e si y. S udies ha ocus on eshwa e sys ems, show a g ea e decline in gene ic di e si y compa ed wi h s udies ocusing on ma ine habi a s (Figu e 1a; Table S1). F eshwa e sys ems may he e o e be mo e p one o loss o gene ic di e si y when exposed o ishe ies s ess. Figu e 1. Change in he e ozygosi y associa ed wi h ha es ing (a) ish inhabi ing ma ine and esh- wa e (FW) habi a s, (b) o ganized by o de s, and li e his o y ai s, such as (c) pa i y and (d) mig a- ion s a egy (see Table S1 o da a sou ces). A nega i e alue indica es loss o he e ozygosi y a e a ha es ing e en . Dashed line indica es no change in he e ozygosi y. In panels (a,c), shaded a eas ep esen he dis ibu ion o he da a as densi y, and in panels (b,d), da a a e ep esen ed as means and s anda d e o s. Fu he mo e, in ma ine sys ems, he di e ing occu ence o ish popula ions can in- luence hei ca chabili y, dependen on he ishing me hod used, subsequen ly Figu e 1. Change in he e ozygosi y associa ed wi h ha es ing ( a ) ish inhabi ing ma ine and eshwa- e (FW) habi a s, ( b ) o ganized by o de s, and li e his o y ai s, such as ( c ) pa i y and ( d ) mig a ion s a egy (see Table S1 o da a sou ces). A nega i e alue indica es loss o he e ozygosi y a e a ha es ing e en . Dashed line indica es no change in he e ozygosi y. In panels ( a , c ), shaded a eas ep esen he dis ibu ion o he da a as densi y, and in panels ( b , d ), da a a e ep esen ed as means and s anda d e o s. Fu he mo e, in ma ine sys ems, he di e ing occu ence o ish popula ions can in lu- ence hei ca chabili y, dependen on he ishing me hod used, subsequen ly in luencing ulne abili y o gene ic loss. Fo example, a awle ishe y will likely ha e a g ea e impac on ben hic ish, whils long lines will a ge pelagic ish. In e es ingly, mo e s udies show ha ben hopelagic ish a e mos ulne able o declines in gene ic di e si y ollowing Fishes 2023,8, 510 6 o 14 ishe ies s ess (Table S1), po en ially because hey li e close o he bo om o he ocean whe e ishing me hods such as awling can cause signi ican damage o hei habi a and cause di ec mo ali y [72]. 3.2. La i ude Species di e si y, unc ional di e si y and gene ic di e si y dec ease wi h la i ude because o pos glacial coloniza ion [ 73 , 74 ]. This c ea es a g adien in species numbe , such ha species di e si y is g ea es a he equa o [ 75 , 76 ]. As a esul , ishing p essu e could be expec ed o be mo e in ense a he equa o due o a high numbe o ishing communi ies and species. Howe e , his is no he case, as ishing ho spo s in Eu ope, No h Ame ica, and China skew his pa e n. Because no he n (and pola ) popula ions demons a e lowe le els o gene ic di e si y han sou he n ones, high ishing p essu e in hese a eas migh ha e g ea e impac on gene ic di e si y han an icipa ed [ 77 ]. Shi ing baseline e e s o he phenomenon o how people’s pe cep ions, o example, o gene ic di e si y (o biodi e si y), change o e ime based on hei own expe ience, memo y, o knowledge (e.g., [ 78 ]). Fo example, people may no ealise how much gene ic di e si y has been los in ce ain species o popula ions because hey ha e no e e ence poin o compa e wi h he pas [ 79 ]. This means we should ca e ully conside he imescale o ishe ies, and a wha poin s loss o indeed no loss o gene ic di e si y is obse ed. This can esul in a lack o awa eness o conce n o conse a ion and ishe ies managemen [80]. 3.3. Habi a Complexi y Habi a ange and complexi y a e impo an ac o s in luencing a ish popula ion’s ulne abili y o ishe y s ess. Isola ed, small ish popula ions a e mo e p one o he loss o gene ic di e si y han la ge, well- connec ed popula ions [ 81 ]. Connec i i y o a habi a is c ucial in main aining gene ic di e si y, as i allows o gene ic eco e y h ough mig a ion [ 8 ]. Fu he mo e, a anging, panmic ic species a e mo e likely o ha e si es o e ugia om ishe ies, allowing o a eas o high gene ic di e si y ha can hen con ibu e o he o e all popula ion h ough mig a ion. Mo eo e , physical ba ie s can inhibi connec i i y o popula ions, pa icula ly in eshwa e en i onmen s whe e lakes and i e s can become cu o . In ole ance o ce ain en i onmen al condi ions such as salini y, oxygen, and empe a u e can also c ea e ba ie s o connec i i y. Fo example, Vi o ino e al. [ 82 ] s a e ha A apaima gigas li es in len ic wa e s, and a e in ole an o lo ic en i onmen s ha ac as ba ie s o dispe sal, which may inc ease his species’ suscep ibili y o loss o gene ic di e si y due o lack o e ugia and mig a ion oppo uni y. When p edic ing he po en ial loss o gene ic di e si y induced by ishing, a ious ac o s o he han ishing in ensi y, selec i i y, and ype o gene ic ools used, con ibu e. Unde wa e habi a ype, condi ion, and complexi y can be di icul o always de e mine accu a ely. Howe e , s udies sugges ha hese can possibly magni y he a e a which ishe ies can deg ade gene ic di e si y and, he e o e, hey should be conside ed. 4. Popula ion Demog aphy 4.1. Popula ion Size and Range La ge popula ions a e usually less ulne able o andom gene ic d i and he e o e gene ic di e si y is less likely o be deg aded unde in ense ishing s ess. Indeed, some ha e e en sugges ed ish s ocks a e so la ge ha e en collapsed popula ions a e comple ely esis an o loss o gene ic a ia ion h ough andom gene ic d i [ 83 ]. Howe e , e ec i e popula ion size (N e ; i.e., he numbe o indi iduals ha de e mines gene ic cha ac e is ics, such as allele equency) is o en signi ican ly smalle han he ac ual numbe o ish in a popula ion (census popula ion size, N; [ 84 ]). I was he e o e o en assumed ha gene ic bo lenecks we e a e in la ge ish popula ions when conside ing census popula ion size; howe e , gene ic d i is de e mined by he e ec i e popula ion size ha is many ac o s lowe [ 15 ]. Some au ho s ha e e en sugges ed ha educ ion in allele di e si y as a esul o o e ishing may be mo e in ense in la ge popula ions han small ones [ 85 ]. When a Fishes 2023,8, 510 7 o 14 popula ion is ha es ed down o low numbe s, i s inb eeding coe icien inc eases (i.e., gene ic di e si y dec eases), inb eeding dep ession occu s, i ness is educed oge he wi h he popula ion’s e olu iona y po en ial, and he popula ion can e en ually be des ined o ex inc ion [86]. In addi ion o popula ion size, i s ange can u he de e mine ulne abili y o ishe ies exploi a ion. A widely dis ibu ed species such as una (Thunnus hynnus) is mo e likely o be esis an o gene ic loss caused by ishe ies due o po en ial e ugia in he en i onmen and g ea e habi a connec i i y [ 23 ]. Con e sely, a na owly dis ibu ed species may be mo e p one o gene ic loss because gene ic di e si y canno be main ained by e ugia u i- liza ion and ebuil h ough mig a ion [ 8 ]. Fo example, Maugean ska e (Zea aja maugeana) is endemic o Tasmania, has a na ow ange, is endange ed, and has su e ed om he loss o gene ic di e si y, likely due o a combina ion o ishing and en i onmen al change [87]. 4.2. Sex Ra io Fishing egimes o en a ge he la ge ish in a popula ion, which no only in luences body size and ep oduc ion di ec ly, bu also leads o sex a io al e a ion in sexually dimo phic species [ 38 , 88 ]. In ac , “sex-selec i e” ishe ies can exace ba e he loss o gene ic di e si y by hampe ing ep oduc ion di ec ly by making he o he sex a e, hence lowe ing he N e [ 89 ]. Fo example, in he Gul o Mexico, popula ions o ambe jack (Se iola dume ili) ha e a emale-skewed sex a io, which is likely due o ca ch p e e ences in he egion: emales a e a mo e alued ca ch because hey a e signi ican ly la ge han males, making o a mo e p o i able ca ch [ 90 ]. Fu he mo e, Righi e al. [ 38 ] showed ha unde ishing s ess, male swo d ish (Xiphias gladius) became mo e p e alen in he popula ion as a esul o ishe men a ge ing he la ge emales, leading o losses in gene ic di e si y. A skewed sex a io is a p oblem in all sexually dimo phic ish species ha a e being exploi ed, as he la ge sex is mo e likely o be cap u ed. This can lead o gene ic loss and e en o ex inc ion e en s i he ca ch a e is ex eme. To p e en ishe ies o lead o skewed sex a io, a maximum size limi could be help ul in p o ec ing he po en ially la ge sex ( ypically emale). Howe e , e en mo e s ingen managemen measu es, such as pe manen ishe ies closu e can be e ec i e only when implemen ed in he long e m. A demog aphic eco e y o a ma ine ee ish ook 30 yea s o seasonal ishe ies closu e [ 91 ]. A gene ic eco e y likely akes much longe . Fu he mo e, es ima ing popula ion sizes (census o e ec i e) o o iginal s anding gene ic di e si y can be challenging. Ye , hese wo popula ion-le el cha ac e is ics a e impe a i e i we aim o eliably p edic he a e and magni ude a which ishe ies can induce loss o gene ic di e si y. 5. Li e His o y and Beha iou S udies based on he o e ha es ing o popula ions a e unsu p isingly based on he mos comme cially impo an species, such as cod (Gadus mo hua) and he ing (Clupea ha engus). This leads o an inhe en bias on he li e his o ies and demog aphy o hese s udies. Cod, o example, ha e massi e, in e connec ed popula ions, wi h ex emely high li e ime ecundi y and aking a ela i ely long ime o ma u e. Ancho y and sa dine, on he o he hand, each ma u i y apidly (1–2 yea s) bu ha e ewe spawning e en s. Fu he con as ing a e species such as sha ks and ays ha a e o en e y long li ed, bu wi h low ecundi y. Fish li e his o y, physiology, and beha iou a e ex emely a iable amongs species and, in ui i ely, he e ec o ishe ies on loss o gene ic di e si y will as ly di e . S udies on species which each a la ge body size and ha e long li e spans ha e demons a ed a ishe ies-induced loss o gene ic di e si y, e.g., [ 33 , 38 , 48 ]. Howe e , he same is e iden o small as -li ing species (e.g., [ 92 , 93 ]). Va ia ion exis s in he li e a u e be ween axonomic g oups (Figu e 1b), so deepe explo a ion in o li e his o y ai s is equi ed o unde s and pa e ns o gene ic loss. Fishes 2023,8, 510 8 o 14 5.1. Li e His o y In ensi y o ishe y s ess may a ec ish di e en ly depending on hei ep oduc i e s a egy, as a pelagic ba ch spawne wi h la ae ha dispe se o e as dis ances, such as he ing, may ha e a g ea e chance o main aining gene ic di e si y han species ha lay eggs on o a subs a e [ 94 ]. The la e may be pa icula ly ulne able o awling and o he des uc i e ishe y me hods [ 95 ], as ishe ies will al eady cause high mo ali ies a he egg s age. Fu he mo e, ish ha a e b oadcas spawne s (i.e., spawning con inues o se e al subsequen mon hs and a els a g ea e dis ance), such as una and sa dines, will likely ha e lowe egg mo ali y a e caused by ishe ies, whils in con as , ben hic spawne s ha lay in close p oximi y, a aching eggs o he ben hos, will be p one o he same a ge ed ishing (e.g., cod and plaice), especially des uc i e me hods such as awling, esul ing in highe egg mo ali y and hence an indi ec ly g ea e loss o gene ic di e si y. Rep oduc ion in ish can be b oadly classi ied in o wo ca ego ies: semelpa ous (a single ep oduc i e e en du ing li e ime) and i e opa ous (mul iple ep oduc i e e en s). Semelpa ous ish a e hough o be mo e p one o loss o gene ic di e si y as hey ely on a singula ep oduc i e e en , so ep oduc i e ou pu is dependen on he a ailable pa ne a he ime o ep oduc ion, as well as o sp ing su i al being dependen on he empo ali y o ep oduc ion [ 96 ]. Fo example, ep oduc ion may coincide wi h an en i onmen al s esso o indeed an in ense ishe y e en . In con as , i e opa ous ish sp ead hei ep oduc i e ou pu ou , and a e less likely o be a ec ed by a singula en i onmen al o ishing e en . Species, such as many salmonids, ha spawn once a yea a a speci ic loca ion could be ex emely ulne able o ishe ies i i a ge s spawning popula ions. Fishe ies ha e a ge ed he spawning s ocks o ba ed sand bass (Pa alab ax nebuli e ) and kelp bass (Pa alab ax cla h a us), esul ing in la ge-scale popula ion loss [ 97 ]. Clea ly, ishe ies ope a ing on spawning g ounds, pa icula ly in hose o semelpa ous ishes, can e y e ec i ely educe popula ion sizes and he e o e gene ic di e si y. Howe e , e idence in he li e a u e sugges s i e opa ous ish a e mo e p one o loss o gene ic di e si y (Figu e 1c), hough his could be due o lack o s udies on semelpa ous ish, and indeed i is a a e li e his o y s a egy. Fu he mo e, ishe y closu es du ing spawning season a e nowadays ela i ely common and ha e been sugges ed o con ibu e o sus ainable ishing [98]. Body size has been shown o display a nega i e ela ionship wi h gene ic di e si y [8,99]. As a esul , la ge indi iduals and la ge species a e mo e likely o ha e lowe di e si y, due o body size and ca ch being ela ed o popula ion abundance [ 99 ]. This may esul in o e ished popula ions o smalle indi iduals showing no appa en loss in gene ic di e si y, bu which ha e los c ucial a e alleles ela ed o g ow h and i ness. Fu he mo e, la ge ish a e usually mo e ep oduc i ely success ul in many species, p oducing mo e and la ge eggs [ 100 ]. Mo eo e , la ge emales o en disp opo ionally con ibu e o ec ui men ; he e o e, loss o he la ges indi iduals may esul in a educ ion in he g ow h and ecundi y o he popula ion [ 15 ]. Howe e , con e sely, he emo al o la ge ish ha disp opo iona ely con ibu e o he popula ion may enhance gene ic di e si y due o he inc eased ep oduc i e success o mo e, smalle indi iduals. As such, li e his o y s a egy as a p edic o o he magni ude o ishe ies-d i en loss in gene ic di e si y is no s aigh o wa d and likely in e ac s wi h o he ai s and ac o s. When examining li e his o y s a egies mos ulne able o ishing, an impo an concep is /K-selec ion [ 101 ]. K-selec ed species a e la ge, ma u e la e, and p oduce ela i ely ew o sp ing; as such, hei popula ion size, and hence gene ic di e si y, may be mo e a ec ed by ishing, as o example demons a ed in he o ange oughy (Hoplos e hus a lan icus; [ 48 ]). In con as , -selec ed species cha ac e ized by small body size, ea ly ma u i y, and high ecundi y may be mo e du able o ishe ies s ess, as hey ha e highe popula ion g ow h a es and may be less likely o expe ience gene ic loss. Howe e , ish a e di icul o ca ego ise in o /K-species, as many o hem do no s ic ly ollow he de ini ions. Fo example, cod can be desc ibed as a K-species because i has a la ge body size and ma u es la e, a he age o i e o eigh yea s. Howe e , i is highly ecund and can spawn mo e han 10 million eggs du ing a spawning season [ 102 ]. He e, we canno