Aquatic Mammals 2011, 37(3), 227-235, DOI 10.1578/AM.37.3.2011.227 Population Genetics of the Monk Seals (Genus Monachus): A Review Jennifer K. Schultz Hawaii Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawaii, PO Box 1346, Kaneohe, HI 96744, USA E-mail: [email protected] Summary (M. monachus), and Hawaiian (M. schauinslandi) monk seals. There are few distinguishing morpho- Monk seals (genus Monachus) are among the logical characters among the species (Scheffer, most endangered mammals in the world, with 1958), and the genus appears to be monophyletic. all species sharing a similar history of anthropo- Phylogenetic analyses of the two extant species genic overexploitation. Reductions in population (M. monachus and M. schauinslandi) at mito- abundance have been accompanied by the loss of chondrial DNA loci indicated deep divergence genetic diversity in Mediterranean (M. monachus) between Mediterranean and Hawaiian monk seals and Hawaiian (M. schauinslandi) monk seals. and a mid-late Miocene origin of the lineage Both species are characterized by extremely low (Davis et al., 2004). Sequencing one nuclear and variability at all genetic markers tested to date, three mitochondrial genes, Fyler et al. (2005) esti- including microsatellite loci, the mitochondrial mated the date of divergence to be 10.6 to 11.6 control region, and major histocompatibility com- million years ago (MYA). Citing the occurrence plex class I genes. Genetic variation is partitioned of Monachus fossil representatives in southern differently in the two species. The Hawaiian monk Europe, Fyler et al. described a Tethys origin of seal does not exhibit spatial population structure the genus with initial dispersal to the Caribbean throughout its range in the Hawaiian Archipelago via the North Equatorial Current. Subsequent dis- (FST = 0.00); therefore, it is unlikely that the trans- persal to the tropical Pacific occurred through the location of monk seals will result in genetic incom- Central American Seaway, prior to the emergence patibilities. In contrast, Eastern Mediterranean and of the Isthmus of Panama (de Muizon, 1982). Western Saharan M. monachus populations are Higdon et al. (2007) supported this hypothesis, reproductively isolated (FST = 0.56), though the citing greater morphological similarity between distribution of alleles likely signifies a once con- the Hawaiian and Caribbean species. They also tiguous range sundered by the extirpation of geo- analyzed a large, multi-gene dataset to date the graphically intermediate subpopulations. Given origin of the genus at 11.3 MYA. Arnason et al. the magnitude of genetic differentiation, moving (2006) proposed an alternative phylogeographic Mediterranean monk seals between eastern and hypothesis. Sequencing the whole mitochondrial western populations could result in reduced over- genome of the Hawaiian monk seal and select genes all fitness; additional data is required to assess the of the Mediterranean monk seal, they estimated risk of moving monk seals within a population interspecific divergence at ~13 MYA. Because (e.g., the Eastern Mediterranean). Recent advances the earliest monachine fossil (~14.5 MYA) was in genomics will facilitate future investigation into found in southeastern North America, they pos- the reproductive success of both species and guide tulated that the origin of the genus occurred in managers in their quest to recover Mediterranean the western Atlantic, followed by dispersal to the and Hawaiian monk seal populations. Mediterranean and Hawaii (Arnason et al., 2006). Regardless of which hypothesis best represents Key Words: monk seal, conservation, DNA, Monachus evolution, the species have occupied genetic diversity, pinniped, stock structure their respective ranges for millions of years. The now extinct Caribbean monk seal once Introduction occupied a large range throughout the Caribbean Sea and Gulf of Mexico. Historically, the The genus Monachus is comprised of three spe- Mediterranean monk seal ranged throughout cies: Caribbean (M. tropicalis), Mediterranean the Mediterranean and Black Seas and into the 228 Schultz subtropical East Atlantic Ocean (Johnson & monk seals reside in the Northwestern Hawaiian Lavigne, 1999). Its range is now restricted to pock- Islands, where their habitat is protected as the ets of the northeastern Mediterranean and eastern Papahanaumokuakea Marine National Monument. Atlantic. Hawaiian monk seals are endemic to Since the 1990s, monk seals have also recolonized the Hawaiian Archipelago and are occasionally the main Hawaiian Islands (N = ~152 monk seals; observed at Johnston Atoll, ~1,400 km west of Baker et al., 2011). Hawaii (Antonelis et al., 2006). Such extreme population reductions have All three species have been hunted throughout impacted the diversity and distribution of genetic their respective ranges for meat, oil, and skins such variation within the extant species. The follow- that Monachus seals are among the most endan- ing is a review of published literature on popula- gered of all marine mammals. McClenachan & tion genetics of the Mediterranean and Hawaiian Cooper (2008) estimated that 233,000 to 338,000 monk seals, focusing on genetic diversity, popula- Caribbean monk seals were distributed among 13 tion bottlenecks, and stock structure. Implications colonies prior to discovery and exploitation by for conservation and future directions are also Westerners, beginning with Christopher Columbus addressed. in 1494. The last monk seal was observed in 1952, and the species has since been declared extinct Genetic Diversity (Le Boeuf, 1986). The Mediterranean species has a long history Genetic diversity refers to the extent of variation of exploitation. Monk seal remains found in caves found throughout the genome of a species or pop- occupied by Neanderthals exhibit anthropogenic ulation. It is the raw material upon which natural damage (Stringer et al., 2008). Prehistorical draw- selection acts and is essential to population persis- ings and historical accounts document exploitation tence. Genetic diversity is often assessed at both of the once abundant species since the Stone Age, nuclear and mitochondrial loci (i.e., location of a through the Greek, Roman, and Byzantine periods, coding gene or non-coding DNA sequence). Each and into modern times (Johnson & Lavigne, 1999; individual possesses two alleles at a single nuclear www.monachus-guardian.org). Extirpation along locus; the individual is heterozygous at that locus most mainland Mediterranean coasts has left only if the alleles differ. Mitochondrial loci are mater- three small and isolated populations in remote nally inherited, and each individual generally locations: Desertas Islands of Madeira, Cap Blanc possesses only one form or haplotype. Measures Peninsula in the Western Sahara, and in caves of genetic diversity include polymorphism (P), throughout the northeastern Mediterranean (i.e., the proportion of genetic markers (or loci) which Greece and Turkey). The Western Saharan popu- exhibit more than a single form (or allele); allel- lation was reduced from an estimated 317 monk ism (k), the number of alleles at a given locus; and seals in 1996 to 109 individuals in 1997 after a heterozygosity (H), the percentage of individuals mass mortality event (Forcada et al., 1999). Only in a population or species that possess two differ- 20 to 30 adults reside in the Madeira Archipelago ent alleles at a given locus or averaged over all (Pires et al., 2008). The largest population con- loci. While polymorphism and allelism reflect raw sists of 250 to 350 individuals in the eastern genetic variability, heterozygosity is a measure Mediterranean Sea (Dendrinos et al., 2008). of how existing diversity is partitioned among Little is known regarding the first human inter- individuals. actions with the Hawaiian monk seal. Remains found at an archaeological site in the main Microsatellite DNA Hawaiian Islands, radiocarbon dated to 1400 to Mediterranean and Hawaiian monk seals exhibit 1750 AD , suggest that early Hawaiians harvested low diversity at all genetic markers tested to date, monk seals (Rosendahl, 1994). Monk seals had including microsatellite loci—that is, tandemly been extirpated from the main Hawaiian Islands repeated regions of nuclear DNA that are gener- prior to the arrival of the first Western explorers in ally characterized by high variability. Gemmell the 18th century. Western exploration of the unin- et al. (1997) surveyed the utility of 20 microsat- habited Northwestern Hawaiian Islands begin- ellite loci across 18 pinniped species (Table 1). ning in 1805 led to the discovery and exploitation Twelve of the 20 loci were polymorphic in the of the species (Ragen, 1999). A minimum of 23 Mediterranean monk seal (P = 0.60), and allelism individuals survived at the nadir of the hunting- was low (k = 1 to 6, kave = 2). Only three of the 20 induced bottleneck (c. 1893; Schultz et al., 2009). loci were polymorphic in the Hawaiian monk seal Despite a partial recovery by the mid-20th cen- (P = 0.15); allelism was also low (k = 1 to 4, kave = tury, population abundance is currently in decline. 1.25). Though limited in scope (only four and five At present, less than 1,200 Hawaiian monk seals Mediterranean and Hawaiian monk seals were ana- remain (Carretta et al., 2009). The majority of the lyzed, respectively), the study is important because mark ers,di (ersity v able 1. of alleles ) and poly - of 20 ), a v ) for T Comparisonsat a of genetic