doi:10.1111/j.1420-9101.2006.01251.x Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes J. E. MANK Evolutionary Biology Centre, Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden Keywords: Abstract prezygotic isolation; Evolutionary theory predicts that sexual selection may increase taxonomic sister-clade comparisons; diversity when emergent mating preferences result in reproductive isolation taxonomic diversity. and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P ¼ 0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis. The theory linking sexual selection (as a proxy for Introduction mating preferences) and cladogenesis has been anecdo- Changes in mating preferences can theoretically lead to tally invoked to explain observed patterns of diversity in speciation events if the emergent mating preferences some clades of ray-finned (actinopterygiian) fishes result in assortative mating and reproductive (prezygotic) (McMillan et al., 1999; Mendelson, 2003). The explosive isolation. Increased prezygotic isolation would be expec- radiation of the cichlid fishes has been repeatedly linked ted to accelerate taxonomic diversification compared to mating preferences for sexually selected behavioural with post-zygotic barriers to gene flow, which can and morphological ornaments (Dominey, 1984; Knight require long periods of time to accumulate. This suggests et al., 1998; Maan et al., 2004). Sexual selection via that sexually selected traits, common manifestations of mating preference has been documented in shaping a the pressures of mating preferences, may be associated variety of traits in the ray-finned fishes, including with taxonomic diversification (Darwin, 1871; Lande, dichromatism (Endler, 1980; Houde & Endler, 1990), 1981, 1982; West-Eberhard, 1983). This correlation has breeding tubercles (Kortet et al., 2003, 2004) and elon- been supported by some large-scale comparative analy- gated fins (Basolo, 1990; Meyer, 1997). Despite these ses, primarily in birds and invertebrates (Barraclough clear documentations linking mating preferences and et al., 1995; Gleason & Ritchie, 1998; Masta & Maddison, sexually selected traits (usually, though not always 2002; Polak et al., 2004). displayed in males) for species or small clades of Actin- opterygii, some comparative studies in the ray-finned Correspondence: Judith E. Mank, Evolutionary Biology Centre, Department fishes have failed to uncover the expected manifestations of Evolutionary Biology, Uppsala University, Norbyva¨gen 18D, SE-752 36 Uppsala, Sweden. of female preference (Ritchie et al., 2005; Mank et al., Tel.: +46 (18) 471-6461; fax: +46 (18) 471-6310; 2006), casting doubt as to pervasiveness and magnitude e-mail: [email protected] of female preference through the clade. ª 2006 THE AUTHOR 20 (2007) 597–602 JOURNAL COMPILATION ª 2006 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 597 598 J. E. MANK Additionally, the relative importance of sexual selec- For the sister families with some degree of manifest tion in explaining patterns of actinopterygiian diversity is sexual selection, I searched numerous field guides, unclear as several other unrelated factors have been species accounts, and aquarium references for descrip- recently identified as promoting diversification in this tions of sexually selected traits (available in the Supple- clade. Changes in genomic architecture (Hoegg et al., mental materials) in all currently taxonomically 2004; Mank & Avise, 2006a), key innovations such as recognized species (Eschmeyer, 1990, 1998; Froese & internal gestation (Lydeard, 1993; Mank & Avise, 2006c) Pauly, 2004). The sexually selected traits included here and antifreeze genes (Bargelloni et al., 1994; Eastman & have been used in previous comparative studies of sexual McCune, 2000; Near et al., 2004), as well as vicariance selection in the Actinopterygii (Mank et al., 2005, 2006; (Murphy & Collier, 1996, 1997; Hurwood & Hughes, Mank & Avise, 2006b; Mank, in press), and have been 1998; Planes & Fauvelot, 2002; Near et al., 2003) have all shown in the clade to be the result of mating preferences. been demonstrably linked to increased cladogenesis in These traits include extended or elongate fins or rays the ray-finned fishes. It is therefore likely that mating (Harrington 1997; Marcus & McCune 1999; Kuwamura preferences, if a major factor at all, act in combination et al. 2000), breeding tubercles (Kortet et al., 2003, 2004), with other unrelated causes to create the current patterns and sexual dichromatism (Reimchen, 1989; Houde & in actinopterygiian diversity. Endler, 1990; Stott & Poulin, 1996; Amundsen & Despite the evidence for and against sexual selection Forgren, 2001). I omitted from this analysis sexually as a driver of diversification in ray-finned fishes, the dimorphic traits that may be the result (at least partially) theory has not been tested across the clade, probably of natural selection, such as body-size dimorphisms because of a combination of problems with the under- (Hamon & Foote, 2005; Schutz & Taborsky, 2005) and lying phylogeny and the difficulty in gathering suffi- gonopodia (Langerhans et al., 2005). The nature of cient data on sexually selected traits. The recent ichthyological data also prevented incorporation of some construction of a well-resolved provisional supertree putatively sexually selected traits that are simply too (Mank et al., 2005) for the Actinopterygii has partially poorly documented in a wide variety of actinopterygiian resolved this problem and provides the necessary phy- species, such as olfactory cues (Shohet & Watt, 2004; logenetic framework for a broad-scale comparative Milinski et al., 2005). analysis. This supertree framework, in conjunction with Numerous fish species are described on the basis of a numerous species accounts and field guides, offers the single preserved type specimen, often collected long first opportunity to test the role of mating preference in before the taxonomy is evaluated and described. As promoting taxonomic diversification across the Actin- colour patterns often rapidly fade in preservation jars, it opterygii. Using sister clade comparisons identified from is not possible to ascertain from preserved museum type the supertree, I tested the relationship between the specimens whether sexual dichromatism, the most com- presence of sexually selected traits, a proxy for mating mon manifestation of sexual selection in fish, exists. In preference, and increased diversification in the ray- order to avoid underestimating the incidence and finned fishes. importance of sexual dichromatism in the dataset, I did not use species accounts based solely on preserved Materials and methods specimens. This strategy presented an alternative prob- lem, as some families are described almost entirely based From the actinopterygiian supertree (Mank et al., 2005), on pickled individuals. I therefore removed all sister a 90% consensus tree from 25 000 most parsimonious families that were insufficiently characterized (< 10% of trees, I identified all potential monophyletic sister fam- recognized species described in detail) from further ilies. Sister families are pairs of families that are taxo- analysis. nomically more related to one another than they are to There is not yet a complete and comprehensive any other family, and are equally old by definition molecular phylogeny for the Actinopterygii, or a large (Cracraft, 1981). This type of sister clade comparison sub-clade, with which to estimate branch-lengths and therefore automatically corrects for shared ancestry and divergence times. Additionally, it is not possible to divergence time in the assessment of any correlative estimate branch lengths and divergence times on the relationship. current actinoptergyiian supertree (Mank et al., 2005) For each of these sister taxa, I first assessed whether because of the amalgamated nature of the underlying there were any manifest sexually selected traits, using a dataset. I therefore analysed the identified sister families family level compendium (Breder & Rosen, 1966). Sister according to the recommendations of Barraclough et al. families that completely lacked evidence of sexual (1995), Nee et al. (1996) and Vamosi & Vamosi (2005). selection were removed from any further analysis. These For each sister family, I calculated the proportion of sister clades are uninformative regarding the relationship species that exhibited sexually selected traits, as well as between manifest sexual selection and diversification determined