Hybridism (marine mammals)

 

Apeciation is assumed to be a function of genetic divergence caused by reproductive barriers between gene pools ? (i.e., different populations). Traditionally, species are either allopatric or sijmpatric. In the case of sympatric species mechanisms such as temporal segregation, behavioral differences, and gametic incompatibilities ensure reproductive isolation. Hybridization denotes the successful mating between two individuals from different and reproductively isolated gene pools accepted as species. Hybridization is observed frequently among higher plants, but only rarely among vertebrates. Within mammals, hybrids have been recorded in a number of marine as well as terrestrial species. The evolutionary consequences of such hybrids vary depending on the frequency, the degree of genetic differences between the parental species, mating system, and the ecological circumstances.

The examination of hybrids has always attracted much attention, as such incidences and their frequency might provide clues to reproductive behavior, dispersal capabilities, and phylogenetic relationship of species. As might be expected, hybrids are more common within genera where the different species have similar life histories and habitat requirements. When the frequency of hybridization is low, the fitness of the hybrids is generally low as well and hybrids usually are nonviable or sterile and thus do not represent a threat to the genetic constitution of the parental species. However, as the frequency of hybridization increases, so may the number of viable and reproductive hybrids, which in turn might cause the breakdown of previous reproductive barriers between the two species. One evolutionary consequence of such a scenario is introgression. A recent well-documented example of this is the high incidence of coyote genes in what morphologically seem to be gray wolves observed in North America (Lehman et al, 1991). The ultimate evolutionary consequence of introgression is the extinction of the species whose genome is being replaced by the other.

With regard to marine mammals, a total of some 61 cases of alleged hybridization have been described; 40 within Cetacea and 21 within the pinniped Carnivora. Putative hybrids have been observed in captivity as well as in the wild. Most of the marine mammal hybrids reported so far have only been described morphologically. However, molecular techniques have been applied in some cases in order to confirm the identity of hybrids and identify the parental species.

I. Evidence of Mating between Species

Although the theoretical expectation is that male and female genital morphology evolves continuously and thus makes interspecific mating difficult or impossible, attempts of interspecific mating have been observed between pinniped species where no hybrids have yet been reported. Such mating appears to be aggressive, and usually the heterospecific male is much larger than the female. Often the female does not survive such a mating (Miller et al, 1996).

This kind of aggressive interspecific mating was first observed between a male gray seal (Halichoerus grypus) and a female harbor seal (Phoca vitulina) (Wilson, 1975). Later reports of such aggressive behaviors include mating between (i) a male New Zealand sea lion (Phocarctos hookeri) and a dead female New Zealand fur seal (Arctocephalus forsteri) (King, 1983), (ii) a south American sea lion (Otaria flavescens) and a South American fur seal (A. australis) (Miller et al, 1996), (iii) a female California sea lion (Zalophus californianus) and a male Steller sea lion (Eumetopias jubatus) (Miller et al, 1996), (iv) and finally between southern elephant seals (Miroimga leon-ina) and Australian fur seals (A. pusillus) (Miller et al., 1996).

The aggressive mating by sea lions with heterospecific females has been interpreted as “excess of violent sexual selection” (Miller et al., 1996). This aggressive behavior seems to be widespread in the family Otariidae (eared seals), and possibly the number of hybrids is much higher than reported to date.

II. Reported Occurrences of Hybridization in Captivity

Among captive cetaceans, 25 hybrids have been identified, all within the suborder Odontoceti (toothed whales). All hybridizations occurred between seven species of the Delphi-noidea superfamily, where the bottlenose dolphin, Tursiops tmncatus, was one of the parental species in all cases (see Table I, Fig. 1). The majority of these hybrids have not survived. However, a first-generation hybrid between a bottlenose dolphin (T. tmncatus) and a false killer whale (Pseudorca cras-sldens) has given birth twice after mating with a bottlenose dolphin (Duffield, 1998). When these occurrences were reported in 1998, one of the two calves from this second generation was still alive. Finally, within the pinnipeds, hybridization in captivity has been observed within the two families Phocidae (earless seals) and Otariidae (eared seals) (see Table I).

III. Reported Occurrences of Hybridization in the Wild

Probably the most impressive occurrences of hybridization among marine mammals are those identified within the suborder Mysticeti (baleen whales). A total of 11 hybrids among baleen whale species have been reported so far; all of these were captured during commercial whaling operations. In all incidences the parental species involved were a blue (Balaetioptera muscu-lus) and a fin whale (B. physalus). The first report of such anomalous baleen whales was in 1887 by A. H. Cocks (1887), who recorded 6 hybrids, or “Bastards,” along the Lapland coast. However, this number is likely to be an underestimate as the author mentioned that sometimes hybrids were entered in their records as a fin whale instead of “Bastard.” Later, Doroshenko (1970) reported a hybrid between a blue and fin whale, taken in 1965 off Kodiak Island (in the Gulf of Alaska), identified from its exceptional but intermediate morphological traits.

More recently, three anomalous baleen whales, one female and two males, caught during the Icelandic whaling operations between 1983 and 1989 were described morphologically as fin/blue whale hybrids. The parental species of these specimens were later confirmed by molecular analyses of the maternally inherited mitochondrial genome as well as Mendelian-transmitted nuclear genes (Arnason et al., 1991; Spilliaert et al, 1991). Interestingly, the female Icelandic fin/blue whale hybrid was in her second pregnancy. Molecular analyses of the fetus found that it was the result of a mating between the hybrid mother and a male blue whale. Finally, a fin/blue whale hybrid caught off northwest Spain in 1984 was identified morphologically, and subsequent molecular analyses found the maternal species to be a blue whale and the paternal species a fin whale (Berube and Aguilar, 1998).

Within the Odontoceti, the first three hybrids described were from a stranding on the West Coast of Ireland in Blacksod Bay (Fraser, 1940). Morphological analysis concluded that the three stranded specimens were hybrids from matings between bottlenose and Risso’s dolphins (Grampus griseus). The occurrence of as many as three hybrid individuals in the same stranding, each a cross of the same parental species, is highly unusual given the overall low rate of hybridization among cetaceans per se. For the same reason, Fraser himself first thought the hybrids to be a novel species rather than hybrids. Since the stranding in Blacksod Bay, only a single incidence of hybridization in the wild has been reported within the familv Delphinidae. This specimen was caught by fishermen off the Peruvian coast and determined to be a hybrid between common (Delphi mis capensis or delphis) and dusky dolphin (Lagenorhtjnchus obscurus) based on its morphology (Reyes, 1996).

TABLE I

Reported Occurrences of Captive Hybridization


Families involved

Species

Parental role

Method of detection

Reported number of hybrids

Reference

Delphinidae

T. iruncaius

Dam

Morphological

13

Shimura et al. (1986). Sylvestre and Tasaka

X G. griseus

Sire

and molecular

(1985)

T. truncatus

Dam

Morphological

2

Duffield (1998)

X D. delphis

Sire

T. truncatus

Dam

Morphological

1

W. Perrin, personal communication

X D. capensis

Sire

T. truncatus

Dam

Morphological

6

Duffield (1998). Nishiwaki and Tobavama (1982)

X P. crassidens

Sire

S. bredanensis

Dam

Morphological

1

Dohl et al. (1974)

X T. truncatus

Sire

G. macrorhynchus

Dam

Morphological

2

Duffield (1998)

X T. truncatus

Sire

Phocidae

P. hispida

Dam

Morphological

1

King (1983)

X H. grypus

Sire

Otariidae

C. ursinus

Dam

Morphological

1

Duffield (1998)

X Z. califomianus

Sire

Z. califomianus

Dam

Morphological

1 +

King (1983)

X A. pusillus

Sire

Z. califomianus

Dam

Morphological

1

King (1983)

X O. flavescens

Sire

In 1990, an anomalous whale skull was collected in Disko Bay at west Greenland. The morphological characteristics of this skull were intermediate between those of adult narwhal (Monodon monoceros) and beluga (Delphinaptcrus leucas), and the authors hypothesized that the specimen was likely a narwhal-beluga hybrid (Heide-J0gensen and Reeves, 1993).

The most recent case of hybridization reported within Odon-toceti is a female fetus recovered from a dead Dall’s porpoise (Phocoenoides dalli). Morphological and molecular analyses determined the fetus as a cross between a Dall’s and a harbor porpoise (Phocoena phocoena) (Baird et al. 1998).

The most common occurrence of hybridization in pinnipeds is between the sub-antarctic (Arctocephalus tropicalis) and the Antarctic fur seal (A. gazella) (Table II). Based upon the population estimates for each of the two species and the frequency of hybrids, the magnitude of hybridization has been estimated to represent 9.3 and 0.1% of the A. gazella and A. tropicalis populations, respectively (Kerlev, 1983).

IV. Evolutionary Implications of Hybridization

The evolutionary significance of hybridization is not known, but hybridization does provide an opportunity for gene flow between otherwise isolated gene pools, e.g., exchange of adaptive traits. Among marine mammals, hybridization has been shown to occur between a variety of species (Tables I and II). However, the overall rate of hybridization appears to be quite limited, and no cases of introgression have yet been identified. The apparent scarcity of hybrids may not be a true reflection of the actual rate, i.e., it is possible that hybrids simply are overlooked or not reported (during commercial or subsistence whaling) in order to avoid sanctions for killing protected species (e.g., blue whales). Furthermore, the identification of hybrids so far has relied primarily on morphological characters, which usually require that the specimen be killed. However, the introduction of nonlethal methods (Lambertsen, 1987) to obtain the necessary tissue for molecular methods as skin biopsies from free-ranging cetaceans makes it a simple task to identify hybrids today.

Marine mammals are genetically relatively similar. In comparison, the level of genetic divergence between the fin and the blue whale is similar to that observed among human (Homo sapiens), chimpanzee (Pan troglodytes, P. paniscus), and gorilla (Gorilla gorilla) (Arnason and Gullberg, 1993). Even within all cetaceans, where mysticetes and odontocetes probably diverged some 40 million years ago, nearly all species have the same number of chromosomes (2n=44; a few have 2n=42) and similar karyotypes. Among the pinnipeds, more variation in chromosome number has been detected; the number of diploid chromosomes can be from 32 to 36 (Arnason, 1990). The relatively similar genetic background and often sympatric existence (in feeding or breeding range) among closely related marine mammals would seem to favor hybridization. However, as mentioned earlier, hybridization is rare, and between species where several hybrids have been observed (such as the fin and the blue whale), the genetic integrity of the parental species appears intact.

TABLE II

Reported Occurrences of Hybridization in the Wild

Families involved

Species involved

Parental role

Method of detection

Reported number of hybrids

Balaenopteridae

B. physalus

Sire and dam

Morphological

11 +

X B. muscidus

Sire and dam

and molecular

 

Delphinidae

T. truncatus X G.griseus

?

Morphological

3

Delphinidae

D. capensis X L. obscurus

?

Morphological

1

Monodontidae

D. leucas X M. monoceros

?

Morphological

1

Phocoenidae

Phocoenoides dalli

Dam

Morphological

1

X Phocoena phocoena

Sire

and molecular

 

Phocidae

C. cristata

Dain

Morphological

1

X Pagophilus groenlandicus

Sire

and molecular

 

Otariidae

A. gazella X A. tropicalis

?

Morphological

15

Otariidae

O. flavescens X A. australis

?

Morphological

?

Hybridization can occur in both natural and captive settings. Instances are more common between closely related taxa, but the ability to hybridize is not always indicative of close phylogenetic affinity. Pictured here is a hybrid between Tursiops and Steno.

Figure 1 Hybridization can occur in both natural and captive settings. Instances are more common between closely related taxa, but the ability to hybridize is not always indicative of close phylogenetic affinity. Pictured here is a hybrid between Tursiops and Steno.

It has been argued that hybrids of the heterogametic sex (males in mammals with a single X and Y chromosome) were most likely to be sterile or nonviable (Haldane, 1922). Since then, evolutionary geneticists have been looking to test this “Haldane’s” rule. Among cetaceans, specifically the family Mys-ticeti, the only two male blue/fin whale hybrids examined to date were both sexually immature despite their relatively high age (Arnason et al., 1991). Although consistent with Haldane’s rule, which has been supported in a number of terrestrial mammals, the small sample size makes it impossible to assess with certainty if the rule applies to marine mammals as well.

The incidence of anomalous marine mammals reported so far has shown that hybridization does occur in captivity as well as in natural settings. Some of these hybrids (mainly in captive animals) have been carried to term and survived. However, only a single case has produced viable calves (unfortunately, the time of birth was not mentioned), of which only one was reported still alive in 1998 (Duffield, 1998). In the case of captive animals, it is difficult to assess if the seemingly low viability of the offspring is related to their hybrid origin or to the general low rate of survival in observed captive-born cetaceans (Van Gelder, 1977). Nonetheless, the observed occurrences of viable and fertile hybrids in captivity suggest that such could happen in the wild. However, to date no offspring of a hybrid has been observed alive in the wild. Whether this is due to our limited ability to detect such hybrids or if indeed (as the lack of introgression indicates) that such viable offspring from hybrids are rare is still an open question.

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