Population discrimination of the French grunt, Haemulon flavolineatum (Desmarest, 1823) between the Campeche Bank and the Mexican Caribbean Sea, inferred by microsatellite loci

Abstract

Genetic structure of the French grunt Haemulon flavolineatum, population was determined in four localities, two located in the Campeche Bank (Cayo Arcas and Alacranes) and two in the Mexican Caribbean (Puerto Morelos and Banco Chinchorro) using microsatellite loci. Intra- and inter-population genetic variabilities, and genetic distances were evaluated. The Monmonier’s maximum-difference algorithm was used to identify population structure and the putative genetic barriers across the oceanographic landscape. Overall expected heterozygosity (He) was lower (0.81) than the observed heterozygosity (Ho = 0.85). Inbreeding index indicated an excess of heterozygotes occur within the whole study area (F${}_{\mathrm{IS}}$ = -0.039); while fixation index denoted genetic significant differences between localities (F${}_{\mathrm{ST}}$ = 0.033). Nei’s genetic distances were wider between Puerto Morelos and Alacranes (0.232), while the narrower were observed between Alacranes and Cayo Arcas (0.106). Monmonier’s algorithm revealed three putative barriers: the first one separated the Campeche Bank from the Caribbean, the second one separated Puerto Morelos from Chinchorro, and finally the third one separated Cayo Arcas from Alacranes. Regional currents allow dispersion of H. flavolineatum between distant populations of the Mesoamerican Barrier Reef and the Gulf of Mexico, but they are not enough to homogenize the populations to form a panmictic population.

Introduction

Most coral reef fishes are known to be relatively sedentary as adults, but they have a pelagic larval phase, in which biological dispersal usually occurs and is regarded as the main genetic interchange mechanism between distant populations of any given fish species, thus structuring their populations at genotypic level (Bergenius et al., 2002, Jackson et al., 2014, Kaspiris, 1970, Leis, 1991, Palumbi, 2003, Sponaugle et al., 2002). In this regard, genetic differences among reef fish populations are known to occur at both large and small spatial scales (Barber et al., 2002, Bowen et al., 2020, Planes et al., 1998, Shulman and Ogden, 1987, Taylor and Hellberg, 2003), in which case a combination of biotic and abiotic factors, such as ocean currents, larval behavior, pelagic larval duration, isolation by distance and historical vicariance, are likely to play important roles in either enhancing long distance dispersal or limiting exchange among populations, contributing to the patterns of genetic connectivity observed in marine systems (Jackson et al., 2014, Piñeros and Gutiérrez-Rodríguez, 2017), in consequence these would determine the spatial scale of the population genotypic structuring (Bernardi, 2000, Cowen et al., 2006, Cowen et al., 2000, Lowe and Allendorf, 2010, Purcell et al., 2009, Villegas-Sánchez et al., 2010).

Even in a fluid ecosystem sometimes gene flow might not be at rates sufficient to homogenize the genetic structure of populations over broad geographical ranges (Fauvelot and Planes, 2002, Green et al., 2015, Palumbi, 2003, Palumbi, 1994, Simpson et al., 2014), especially in sedentary fish species, such as coral reef ones, in which adults are often confined to a limited area by their behavior or the fragmentation of their habitat (Cowen et al., 2000, Leis, 1991). Several studies have been undertaken on coral reef fish and provided divergent outcomes, ranging from panmixia over large areas to local and regional differentiation (Doherty et al., 1995, Jackson et al., 2014, Knutsen et al., 2003, Piñeros and Gutiérrez-Rodríguez, 2017, Planes et al., 2001). Therefore, genetic assessments are encouraged to understand the dispersal levels of marine organisms and their population differentiation (Jones et al., 2010, O’ Conell and Wright, 1997) in order to identify the processes that lead to genetic structure across the ocean scape since it might be crucial for biodiversity conservation and management of marine ecosystems (Antoni and Saillant, 2017, Green et al., 2015).

Conservation biology uses genetic markers and demographic analyses as essential tools for conducting research (Tay et al., 2015). A restrictive dispersion of individuals can cause a decrease in genetic variability and increase differentiation between populations, causing local selection, inbreeding, or gene drift. The genetic structure of a population can be given by larval behavior and by local hydrography (Goldson et al., 2001). Various studies have shown that marine populations are more structured than expected from their dispersal (Cowen et al., 2000, Galindo et al., 2006, Weetman et al., 2006, Wood and Gardner, 2007). Previous studies on the genetic structure of populations have used various techniques such as alloenzymes, mitochondrial DNA, Simple Nucleotide Polymorphism (SNP’s), and microsatellites, obtaining successful results on population structures (O’ Conell and Wright, 1997; (Purcell et al., 2006, Wright and Bentzen, 1994). The genetic characterization of population structure is important in the study of marine species with commercial and ecological importance due to the fact that it indicates whether the populations in wide geographic regions are homogeneous or heterogeneous (Tello Cetina et al., 2013).

In the present study, the genetic structure of the French grunt, Haemulon flavolineatum, population was explored in four localities, two located in the Campeche Bank (Cayo Arcas and Alacranes) within the Gulf of Mexico and other two (Puerto Morelos and Banco Chinchorro) in Mexican Caribbean (northern part of the Mesoamerican Barrier Reef System). Particularly, throughout the study area the ocean circulation is influenced by the Caribbean current that continues towards the Yucatan Peninsula, where it changes its direction to the north becoming the Yucatan Current, part of which is introduced to the Gulf of Mexico and becomes the Loop Current, which joins the Yucatan Current and the Florida Current (Carrillo et al., 2016, Carrillo et al., 2015, Muhling et al., 2013).

H. flavolineatum is distributed from Bermuda and South Carolina to Brazil, including the Gulf of Mexico, West Indies and coasts of central America (Lindeman and Toxey, 2002). It is ecologically important as it provides important energy to reef communities since its one of the main prey species for larger organisms of commercial interest such as groupers and snappers (Appeldoorn et al., 2009, Barden et al., 2014, Mateo et al., 2011). H. flavolineatum is referred to as a group of fish found in greater abundance and biomass in seagrass and coral reefs (Barden et al., 2014, Beets et al., 2003). It has two spawning periods per year, during spring and summer in subtropical climates (McFarland et al., 1985), and it presents two phases during its life history, the first one is larval form, which will last for 14 days (relatively short), and the second one is settlement in coral reefs (McFarland et al., 1985, Shulman and Ogden, 1987). All these mentioned life-history traits of H. flavolineatum would suggest a general belief that this coral reef fish species would reveal significant genetic differentiation among populations at regional spatial scale (Purcell et al., 2006). Therefore, we examined the population differentiation in H. flavolineatum using five polymorphic DNA microsatellites, previously designed for this purpose (Williams et al., 2004), as genetic markers in order to identify the number of distinct groups or populations of H. flavolineatum in the Yucatan Peninsula.